Plant Physiology - The impacts of phosphorus deficiency on ...2018/03/14 · Plant growth under phosphorus deficiency 101 Multiple sets of barley plants (Hordeum vulgare L. cv. Quench)

1

Phosphorus deficiency and photosynthetic machinery 1 Søren Husted - Copenhagen Plant Science Centre, Department of Plant and Environmental 2

Sciences, Faculty of Science, University of Copenhagen, 1871 Frederiksberg C, Denmark – 3

[email protected]. 4

5

The impacts of phosphorus deficiency on the photosynthetic electron transport 6

chain 7

Andreas Carstensen1, Andrei Herdean

2, Sidsel Birkelund Schmidt

1, Anurag Sharma

1, Cornelia 8

Spetea2, Mathias Pribil

1, and Søren Husted

1* 9

1 Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, Faculty of Science, University 10 of Copenhagen, 1871 Frederiksberg C, Denmark 11 2Department of Biological and Environmental Sciences, University of Gothenburg, Box 461, Gothenburg 405 30, 12 Sweden 13 14

One sentence summary: Phosphorus deficiency affects the photosynthetic machinery in barley 15

through a series of sequential events. 16

17

18

Author Contributions 19

A.C., A.H., A.S., C.S., M.P., and S.H. designed the experiments. A.C. and A.H. performed the 20

fluorescence measurements. A.C. and S.B.S. performed the enzyme assays, including the 21

immunoblot analyses. A.S. performed the transmission electron microscopy. All authors 22

participated in data interpretation. A.C. and S.H. drafted the paper, and all authors participated in 23

completing the final version. 24

25

Abstract 26

Phosphorus (P) is an essential macronutrient, and P deficiency limits plant productivity. Recent 27

work showed that P deficiency affects electron transport to photosystem I (PSI), but the underlying 28

mechanisms are unknown. Here, we present a comprehensive biological model describing how P 29

deficiency disrupts the photosynthetic machinery and the electron transport chain through a series 30

of sequential events in barley (Hordeum vulgare). Phosphorus deficiency reduces the 31

orthophosphate (Pi) concentration in the chloroplast stroma to levels that inhibit ATP synthase 32

activity. Consequently, protons accumulate in the thylakoids and cause lumen acidification, which 33

inhibits linear electron flow. Limited plastoquinol (PQH2) oxidation retards electron transport to the 34

cytochrome (Cyt) b6f complex, yet the electron transfer rate of PSI is increased under steady-state 35

growth light and is limited under high light conditions. Under P deficiency, the enhanced electron 36

flow through PSI increases the levels of NADPH, whereas ATP production remains restricted and 37

hence reduces CO2 fixation. In parallel, lumen acidification activates the qE component of the non-38

photochemical quenching (NPQ) mechanism and prevents over-excitation of photosystem II (PSII) 39

and damage to the leaf tissue. Consequently, plants can be severely affected by P deficiency for 40

weeks without displaying any visual leaf symptoms. All of the processes in the photosynthetic 41

machinery influenced by P deficiency appear to be fully reversible and can be restored in less than 42

60 min after resupply of Pi to the leaf tissue. 43

Plant Physiology Preview. Published on March 14, 2018, as DOI:10.1104/pp.17.01624

Copyright 2018 by the American Society of Plant Biologists

www.plantphysiol.orgon September 3, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.plantphysiol.org

2

Introduction 44

Phosphorus (P) is an essential hetero-element in compounds such as ATP, NADPH, nucleic acids, 45

sugar phosphates, and phospholipids, all of which play important roles in photosynthesis 46

(Hammond and White, 2008). Consequently, even marginal P deficiency has a major impact on 47

plant growth and development. It has been estimated that 30% of the world’s arable soils are 48

deficient in P and require P fertilization to improve yields (MacDonald et al., 2011). However, 49

phosphate rock, the source of mineral P fertilizers, is a finite natural resource, and known reserves 50

are projected to last less than a few hundred years at current rates of consumption (Cordell et al., 51

2009; Gilbert, 2009; Walan et al., 2014; Baker et al., 2015). This makes P a strategic natural 52

resource similar to oil, as a few countries control most known reserves. Currently, some parts of the 53

world vastly overuse P fertilization, which causes eutrophication of lakes and coastal waters, 54

whereas limited access to P fertilizer causes crop yield reductions elsewhere (Baker et al., 2015). 55

Phosphorus fertilizer is rapidly immobilized in the soil due to chemical fixation and microbial 56

immobilization; therefore, excessive P application is often required to ensure ample P availability to 57

plants. As a result, less than 20% of P fertilizer added to soils is typically taken up by the crop 58

(Cordell and White, 2015). This obviously low P use efficiency is unsustainable. 59

Orthophosphate (Pi) is a major regulator of carbon metabolism in plants, and P deficiency 60

influences the balance between the synthesis and catabolism of carbon metabolites. Low Pi levels 61

switch the carbon flow to starch accumulation and reduce CO2 assimilation (Heldt et al., 1977). 62

Plants have evolved several responses to balance and stabilize the fluctuating Pi levels that occur at 63

the tissue level in natural environments, such as: (1) altering root morphology and initiating 64

mycorrhizal symbiosis to improve soil exploration for P; (2) activating exudation processes in the 65

rhizosphere to mobilize Pi from the soil; (3) inducing Pi transporter proteins and regulating Pi 66

uptake kinetics; and (4) remobilizing Pi in source organs to meet the requirements of the developing 67

sink tissue (Ramaekers et al., 2010). These responses are supported by homeostatic processes at the 68

cellular level, in which Pi levels are stabilized by mobilization between storage pools in vacuoles 69

and other organelles such as chloroplasts where the photosynthetic machinery is located (Zhang et 70

al., 2014). 71

Homeostatic Pi levels in chloroplasts are controlled by a range of different Pi transporters, which 72

are located in the chloroplast inner envelope or in the thylakoid membrane (Młodzińska and 73

Zboińska, 2016). Three classes of chloroplast Pi transporters have been cloned and characterized, 74

including the PHT2, PHT4, and plastidic Pi translocators. The high-affinity Pi transporter PHT4;1 75

(KM < 400 µM) has been localized in the stroma-exposed regions of the thylakoid membrane, and 76

mediates Pi transport from the thylakoid lumen to the stroma (Guo et al., 2008; Pavón et al., 2008; 77

Yin et al., 2015). A study of Arabidopsis knockout mutants showed that the absence of PHT4;1 78

resulted in a marked decrease in ATP synthase activity; it was assumed that PHT4;1 operates in 79

close proximity to ATP synthase in the thylakoid membrane to maintain sufficient Pi levels for ATP 80

synthesis (Karlsson et al., 2015). It was proposed that an altered supply of Pi in the stroma reduced 81

the ATP levels and thereby reduced CO2 assimilation, but no changes in the photosynthetic 82

machinery composition or electron transport activity were observed (Karlsson et al., 2015). 83

Phosphorus starvation immediately affects CO2 assimilation but does not appear to terminate it, as 84

P-deficient plants typically remain green and do not develop leaf chlorosis. Specifically, P 85

deficiency is believed to affect CO2 assimilation by reducing the ATP-dependent regeneration of 86

ribulose-1,5-bisphosphate (RuBP) in the Calvin cycle (Rao and Terry, 1995; Yan et al., 2015), 87

whereas its effects on the amounts and carboxylation activity of ribulose-1,5-bisphosphate 88

carboxylase/oxygenase (RuBisCO) are less clear (Rychter and Rao, 2005; Reich et al., 2009; 89

Muneer and Jeong, 2015). 90



3

We recently showed that even marginal P deficiency has a marked effect on electron transport 91

between photosystem II (PSII) and photosystem I (PSI) (Frydenvang et al., 2015). An analysis of 92

chlorophyll a fluorescence (OJIP) transients indicated that the I-step in the electron transport chain 93

was markedly affected by P deficiency, and that the change in the fluorescence transient curvature 94

could be used to quantify the bioactive pool of Pi in plants. However, the targets of P deficiency 95

within the thylakoids upstream of ATP synthase remain largely unknown despite decades of 96

research. The objective of this study was to develop a comprehensive biological model of how 97

photosynthesis is affected by P deficiency under physiologically relevant conditions. 98



4

Results 99

Plant growth under phosphorus deficiency 100

Multiple sets of barley plants (Hordeum vulgare L. cv. Quench) were hydroponically cultivated 101

using three different treatments: (1) the control treatment, in which plants were treated with a 102

sufficient nutrient supply throughout the experiment, (2) the P-deficient treatment, in which plants 103

were treated with all nutrients as in the control treatment but with a restricted (low) P concentration, 104

and (3) the P resupply treatment, in which P-deficient plants were supplemented with P 105

concentrations similar to those used in the control treatment at 21 or 25 days after planting (DAP). 106

The plant material was harvested at 28 DAP. Phosphorus deficiency was observed to reduce plant 107

tillering and biomass, whereas it increased anthocyanin accumulation in stems (Supplementary 108

Figure S1). The three different treatments resulted in leaf tissue P concentrations ranging from 109

<1,000 μg P g-1

dry weight (DW) for P deficiency (treatment 2) to >4,000 μg P g-1

DW in the 110

youngest fully-expanded leaves (YFELs) for the control (treatment 1) and P resupply (treatment 3) 111

(Figure 1). We confirmed that the plants had no nutrient deficiencies other than P (Supplementary 112

Table S1). Despite the large range of leaf P concentrations, no visual differences between leaves 113

were observed. 114

115

Chlorophyll a fluorescence measurements revealed phosphorus deficiency 116

Chlorophyll a fluorescence transients (OJIP transients) from the three different treatments revealed 117

a depletion of the I-step for the P-deficient plants (Figure 2A). Before P resupply at 21 DAP in 118

treatment 3, plants subjected to control and P-deficient treatments were easily differentiated when 119

focusing on the I-step. Seven days after P resupply to P-deficient plants (28 DAP), the I-step 120

returned to control conditions, and the flat plateau resembling the I-step was even more distinct than 121

that observed for the control plants (Figure 2A, inset). To demonstrate that P deficiency in plants is 122

highly reversible and that disruptions in electron transport can be rapidly recovered, we infiltrated 123

P-deficient leaf segments with a Pi containing solution by immersion for 60 minutes. The I-step of 124

the OJIP transients in P-deficient plants was highly reversible and displayed a response to P 125

infiltration into leaves in less than 1 h (Figure 2B). The quantum efficiency of PSII (FV/FM) was 126

unable to discriminate between the treatments because all transients reached values close to the 127

theoretical maximum of 0.83. The fluorescence quenching kinetics after reaching the maximum 128

fluorescence (P-step, Figure 2A) was much faster for the P-deficient plants than for the control and 129

P-resupplied plants. The slopes of the fluorescence quenching curves between 2 and 10 s were 130

0.035 ± 0.001, 0.066 ± 0.002, and 0.040 ± 0.002 for the control, P-deficient, and P-resupplied 131

plants, respectively. These results indicated that fluorescence quenching in plants resupplied with P 132

did not significantly differ from that of control plants. Therefore, changes in both the I-step and the 133

fluorescence quenching kinetics appear to be highly valuable for diagnosing P deficiency. 134

135

Inhibition of electron transport to PSI depletes the I-step in the fluorescence transient 136

Chemical inhibitors are commonly used to study electron flow in photosynthesis. We used three 137

different inhibitors to manipulate electron transfer in the YFELs of control plants (Figure 3A). 138

Leaves infiltrated with 3-(3,4–dichlorophenyl)-1,1-dimethylurea (DCMU) exhibited chlorophyll a 139

fluorescence transients that lacked both the J- and I-steps (Figure 3A). DCMU displaces the 140

quinone acceptor QB from its binding site, thereby blocking any further electron transfer 141

downstream of PSII by preventing QA reoxidation (Duysens and Sweers, 1963). Leaves infiltrated 142

with dibromothymoquinone (DBMIB) exhibited transients that lacked the I-step (Figure 3A), 143

similar to those of P-deficient plants (Figure 2A). DBMIB is an artificial quinone that tightly binds 144

to the cytochrome (Cyt) b6f complex, thereby preventing plastoquinol (PQH2) reoxidation 145



5

(Schansker et al., 2005) and preventing electron transport from PQH2 to PSI. Leaves infiltrated with 146

methyl viologen (MV) exhibited distinct transients that lacked the I-step (Figure 3A). When 147

illuminating leaves that have been dark-adapted for more than 10 min, there is a transient restriction 148

in electron flow in PSI because ferredoxin-NADP+ reductase (FNR) is inactivated. This transient 149

block is thought to be important for the development of the I-step kinetics. MV is an effective 150

electron acceptor that strongly competes with ferredoxin for electrons from the FeS clusters in PSI, 151

thereby bypassing the transient block imposed by FNR during dark adaption (Schansker et al., 152

2005). All infiltrations with chemical inhibitors were compared with leaves infiltrated with Milli-Q 153

water as a control. 154

To further demonstrate that fluorescence transients of P-deficient plants lack the I-step due to 155

inhibition of electron transport to PSI, OJIP transients were obtained from two Arabidopsis PSI 156

mutants, psad1-1 and psae1-3, which have pronounced reductions in the levels of the PSI subunits 157

PsaD1 and PsaE1, respectively. These two mutants have markedly impaired photosynthetic electron 158

flow (Ihnatowicz et al., 2004; Ihnatowicz et al., 2007). The transients of both mutants essentially 159

lacked the I-step, which is present in wild-type plants (Figure 3B), which supported the results 160

obtained from experiments with the DCMU, DBMIB, and MV inhibitors (Figure 3A). 161

162

Phosphorus deficiency suppresses the production of ATP and increases the production of 163

NADPH 164

NADP+ is the final substrate for the production of NADPH, and NADPH and ATP are the main 165

products of light-dependent reactions in photosynthesis. The NADP+ concentration was 166

significantly reduced in P-deficient barley plants compared with those in control and P resupply 167

plants (Figure 4A). At 3 days after P resupply (28 DAP) to P-deficient plants, the NADP+ 168

concentration was restored to that in control plants. The opposite trend was present for NADPH, 169

with the NADPH concentration being significantly higher in P-deficient plants than in control and 170

P-resupplied plants (Figure 4B). As for the NADP+ concentration, the same trend was observed for 171

the ATP concentration in isolated thylakoids, although the ATP level in P-resupplied plants was 172

lower than that in control plants (Figure 4C). The orthophosphate (PO43

; Pi) concentration at the 173

whole-leaf level was severely reduced in the P-deficient plants (Figure 4D). The total Pi 174

concentration in chloroplasts isolated after either a dark or light period (Figure 4E, F, respectively) 175

was significantly lower in the P-deficient plants; however, the relative change was lower than that 176

observed at the whole-leaf level. The starch content was significantly higher in P-deficient plants 177

than in control and P-resupplied plants (Figure 4G). These differences in starch contents were 178

visually confirmed using transmission electron micrographs of chloroplasts from control, P-179

deficient, and P-resupplied plants, whereas no striking differences in chloroplast or thylakoid 180

structure were observed (Supplementary Figure S2). 181

We further investigated the P-mediated changes in key photosynthetic proteins by performing 182

immunoblot analysis on thylakoids isolated from 28-day-old YFELs using antibodies against FNR, 183

ferredoxin (FDX1), PsaA, PsaF, Cyt f, D1, and CP43. Visual inspection and quantification of the 184

protein blots confirmed that the different P treatments did not affect the photosynthetic machinery at 185

the protein level (Supplementary Figure S3 and Supplementary Table S2). 186

A severe reduction in stromal P concentration induced by mannose infiltration (Takizawa et al., 187

2008) or by the absence of the chloroplast-localized Pi transporter PHT4;1 (Karlsson et al., 2015) 188

reduced proton flux through ATP synthase and subsequently induced lumen acidification. To 189

determine if this also occurs in plants subjected to P deficiency at physiologically relevant 190

concentrations, we analysed the magnitude and partitioning of the proton motive force (pmf) that 191

drives ATP synthase. The results showed that P-deficient plants had a reduced ATP synthase 192

activity (Figure 5A), which is in agreement with the observed reduced ATP concentrations (Figure 193



6

4C). However, 7 days after P resupply (at 28 DAP), ATP synthase activity was fully restored to 194

control levels. Changes in pmf, which reflect pH differences across the thylakoid membrane (ΔpH) 195

and differences in the electrical potential (ΔΨ), were significantly affected by P deficiency (Figure 196

5B). The pmf in P-deficient plants was essentially exclusively determined by ΔpH (94%), which 197

most probably indicates a highly acidified lumen, whereas the control and P-resupplied plants had 198

pmf values reflecting a balanced distribution between ΔpH and ΔΨ (Figure 5B). Since pmf size and 199

its components were determined from light-dark measurements of the electrochromic band shift 200

(ECS) signal, the pmf size may have been underestimated because the ECS dark relaxation is 201

dependent on the free energy for ATP formation (ΔGATP), which in turn depends on the 202

[ATP]/[ADP]*[Pi] ratio in the chloroplast stroma. However, lumen acidification was further 203

supported by analysing the extended chlorophyll a fluorescence transients (the full OJIP-PSMT 204

curve) (Supplementary Figure S4). At low saturating actinic light intensity (1,000 μmol photons m-2

205

s-1

), a distinct disappearance of the S-M phase was observed for P-deficient plants, which was 206

previously associated with lumen acidification and attenuation of the electron flow from PSII to PSI 207

(Goltsev et al., 2016). 208

Lumen acidification is an immediate signal that triggers feedback regulation of light capture via 209

the energy-dependent quenching (qE) component, being the largest and most rapidly induced 210

component of non-photochemical quenching (NPQ) (Müller et al., 2001). The NPQ measurements 211

for the three treatments again revealed that P-deficient plants differed from control and P-resupplied 212

plants (Supplementary Figure S5). NPQ sharply increased immediately after the onset of 213

illumination in P-deficient plants, and was higher than that for control and P-resupplied plants 214

throughout the entire period of illumination (Supplementary Figure S5A). Furthermore, NPQ 215

relaxation in the dark was slower for P-deficient plants and associated with a reduction in PSII 216

quantum yield (Supplementary Figure S5B). 217

We also directly quantified qE in growth light and at increasing light intensities, which 218

confirmed that this component of NPQ is substantially higher in P-deficient plants across all light 219

intensities (Figure 6A). Moreover, the electron transfer rate through PSII (ETR(II)) was lower 220

across all light intensities in P deficient plants (Figure 6B), whereas the electron transfer rate 221

through PSI (ETR(I)) was higher in growth light, and lower with increasing light intensities 222

compared to the control plants (Figure 6C). Further measurements under steady-state growth light 223

conditions revealed that PSII quantum yield (ɸ(II)), linear electron flow (LEF), and the fraction of 224

open reaction centres (qP) were significantly reduced (Table 1). In agreement with the standard 225

NPQ and qE measurements (Supplementary Figure S5, Figure 6A), NPQt (Tietz et al., 2017) under 226

steady-state growth light conditions was 10-fold higher in P-deficient plants (Table 1). No 227

differences in ETR(I), ETR(II), or state transition (Supplementary Table S3) were observed in low 228

light (60 μmol photons m−2

s−1

). 229

To examine if lumen acidification leads to impaired PQH2 oxidation at the Cyt b6f complex, we 230

measured the redox state of the PQ pool using OJIP transients (Tóth et al., 2007) (Table 2). The 231

fraction of reduced PQH2 was significantly increased for the P-deficient plants relative to the 232

control and P-resupplied plants, indicating a slower oxidation of PQH2 at the Cyt b6f complex. 233

Finally, to confirm that an impaired PQH2 oxidation at the Cyt b6f complex essentially restricts 234

the flow of electrons to PSI (Schlodder and Meyer, 1987), we evaluated P700+

reduction kinetics 235

(Figure 7). P700+

reduction was markedly higher in P-deficient plants than in control and P-236

resupplied plants in growth light conditions (Figure 7A), but clearly not under high light (2200 237

μmol photons m−2

s−1

) conditions (Figure 7B). This result confirms that the electron flow to PSI is 238

severely reduced in P-deficient plants under increasing light intensity (Figure 6B, C). 239

240



7

Discussion 241

Latent P deficiency without any observable leaf symptoms was successfully induced with leaf P 242

concentrations as low as 850 µg P g-1

DW (Reuter and Robinson, 1997), and chloroplast 243

orthophosphate (Pi) concentrations were measured between 20 and 40 nmol mg-1

chlorophyll 244

depending on whether plants were light- or dark-adapted prior to extraction, respectively (Figure 1, 245

Figure 4E, F, and Supplementary Figure S1). This result was fundamentally different from those of 246

previous studies, which induced P-deficient-like conditions by infiltrating leaf segments with 247

mannose to strip the entire leaf Pi pool by irreversible phosphorylation (Takizawa et al., 2008), or 248

used knockout mutants of the Arabidopsis thylakoid membrane Pi transporter PHT4;1 (Karlsson et 249

al., 2015). Unlike previous publications, we quantified the Pi concentration of isolated chloroplasts 250

from P-deficient plants. Such quantification is not trivial, and the obtained values may not exactly 251

reflect the true in vivo values, since some loss of Pi during the extraction process is unavoidable. 252

However, we found it encouraging that Pi concentrations from both light- and dark-adapted 253

chloroplasts showed the same trend relative to the control, P-deficient, and P-resupplied treatments. 254

This provides confidence that the analytical procedure used here is able to reflect the dynamics of 255

chloroplast Pi when plants were exposed to the treatments. 256

The results presented here indicate that the biological mechanisms reflected by the I-step were 257

achieved by adjusting the P availability in the nutrient solution to obtain physiologically relevant P 258

deficiency responses at the whole-plant level. The establishment of latent P-deficient plants 259

successfully induced a series of fully reversible, but marked, disturbances in the electron flow to 260

PSI and the synthesis of ATP and NADPH. This experimental design allowed us to study how the 261

photosynthetic machinery adapts to long-term P starvation and how rapidly it responds to P 262

resupply, and allowed us to construct a biological model summarizing the cascade of events 263

resulting from P deficiency. 264

265

Phosphorus deficiency affects electron transport beyond PQH2 266

Phosphorus deficiency can be detected based on depletion of the I-step from the fast OJIP region of 267

the chlorophyll a fluorescence transient (Figure 2A). In fact, the response is so sensitive to the leaf 268

tissue P concentration that it can be used to accurately predict bioavailable P in both monocots and 269

dicots (Frydenvang et al., 2015). Several hypotheses have been proposed to explain the biological 270

mechanisms underlying the polyphasic OJIP fluorescence curve. However, despite the general 271

agreement that the O-J phase reflects light-driven accumulation of QA (also known as the QA 272

model) (Strasser and Govindjee, 1992), the explanation for the J-I-P phase is still speculative and 273

controversial. The predominant theoretical interpretations of the J-I-P phase include fluorescence 274

quenching by the oxidized PQ pool (Lavorel and Etienne, 1977), light-driven accumulation of QB 275

and QB2

(Strasser and Govindjee, 1992), reduction of QB and PQ by PSII (Srivastava et al., 1995), 276

direct contributions from PSI fluorescence (Franck et al., 2002), and PSI oxidation (Schansker et 277

al., 2005). It has been suggested that the difference in the electrical potential (Δψ) could modulate 278

the I-P phase, and that it largely influences the fluorescence yield of the J-I-P phase (Vredenberg, 279

2004; Antal et al., 2011). 280

The results presented here indicate that the biological mechanisms reflected by the I-step, which 281

is highly responsive to changes in the leaf tissue P concentration, originate from restricted 282

downstream PQH2 oxidation. Measurements of the PQ-pool redox state confirmed an increased 283

fraction of reduced PQH2 in P-deficient plants (Table 2). The I-step disappeared when leaves were 284

infiltrated with DBMIB to inhibit PQH2 oxidation at the Cyt b6f complex, and similar transients 285

were obtained when bypassing the transient FNR block using MV (Figure 3A). Comparable 286

observations were reported in a previous study (Schansker et al., 2005) that infiltrated pea (Pisum 287



8

sativum L.) leaves with DBMIB and MV. The authors stated that a distinct I-P phase required 288

electron transfer beyond the Cyt b6f complex (blocked by DBMIB) and a transient block at the 289

acceptor side of PSI (bypassed by MV). We note that besides inhibition of plastoquinol oxidation at 290

the QO binding site of the Cyt b6f complex, DBMIB might also quench chlorophyll excited states of 291

the PSII antenna, and act as a PSII electron acceptor, thereby decreasing the reduction of the 292

plastoquinone pool (Belatik et al., 2013). However, with the clear differences between infiltration 293

with DCMU and DBMIB (Figure 3A) and because no effects were observed on the quantum yield 294

efficiency (data not shown), we are convinced that DBMIB specifically inhibited plastoquinol 295

oxidation under the conditions given in the present infiltration study. The two Arabidopsis PSI-296

mutants, psad1-1 and psae1-3, also display severely reduced I-steps, which may reflect the 297

pronounced reductions in the PSI subunits PsaD1 and PsaE1, respectively, that markedly impair 298

photosynthetic electron flow (Ihnatowicz et al., 2004; Ihnatowicz et al., 2007) (Figure 3B). 299

These combined results indicate that the inflection at the I-step remains intact when transient 300

equilibrium is attained between PSII-mediated reduction of the PQ pool and its oxidation by the Cyt 301

b6f complex via electron flow to PSI. The further rise to reach maximum fluorescence at the P-step 302

is achieved when PSI electron acceptors are completely reduced due to a transient block caused by 303

temporarily inactivated FNR, which is induced by the dark adaptation performed before the 304

measurements (Stirbet and Govindjee, 2012). Consequently, reduced inflection at the I-step (and 305

eventually elimination of the I-step) reflects slower electron flow to PSI electron acceptors (Stirbet 306

et al., 2014). This was confirmed by analysis of the P700+ reduction rate in similarly dark-adapted 307

plants, which was markedly slower for P-deficient plants than for control plants (Supplementary 308

Figure S6). Previous work showed that the rate-limiting step in electron transport between the two 309

photosystems is determined by PQH2 oxidation at the Cyt b6f complex (Tikhonov, 2014). Electron 310

flow to PSI is reduced when the PQH2 oxidation rate decreases, which reduces the inflection at the 311

I-step. 312

Analysis of steady-state P700+ reduction rates revealed a higher rate of P700

+ reduction in P-313

deficient plants at growth light conditions (Figure 7A), suggesting that P deficiency upregulates 314

electron transfer rates in PSI under continuous growth light (Figure 6C), while PSII is 315

downregulated (Table 1, Figure 6B). Since LEF was down regulated in growth light (Table 1) and 316

given that electron transfer rates in PSI reflect the sum of linear (originating from PSII) and cyclic 317

electron flow (CEF), the results suggest that CEF is upregulated at steady-state growth light 318

conditions in P-deficient plants. Electron transfer rates of PSI remained similar to those of the 319

control in low light (Supplementary Figure S7, Supplementary Table S3), but became highly 320

downregulated in high light (Figure 6C, Figure 7B), when lumenal pH is expected to significantly 321

acidify. 322

323

Phosphorus deficiency alters ATP and NADPH synthesis 324

In contrast to the highly dynamic Pi levels observed at the leaf tissue level, we observed strong 325

homeostatic regulation of the chloroplast Pi pool (Figure 4D, E, F). Phosphorous deficiency resulted 326

in a marked 4-fold decrease in leaf tissue Pi, whereas Pi in isolated chloroplasts was only reduced by 327

approximately 20-40% depending on whether plants were dark- or light-adapted prior to extraction, 328

respectively. These results suggest that vacuoles contain a storage pool of non-metabolic Pi under 329

adequate P conditions, whereas most of the Pi is sequestered in the metabolic pool in chloroplasts 330

under P-deficient conditions (Lauer et al., 1989). Three Pi transporter families are localized in the 331

chloroplast to supply Pi in the stroma, where PHT4;1 is the only transporter localized in the 332

thylakoid membrane. Furthermore, a limitation in ATP synthase and reduced growth has only been 333

demonstrated for PHT4;1 mutants (Karlsson et al., 2015). PHT4;1 mediates the availability of Pi for 334

ATP synthesis in the chloroplast stroma (Karlsson et al., 2015), and it is likely that the Pi 335



9

concentration in chloroplasts is regulated by effective phosphate homeostasis to maintain ATP 336

synthesis and drive the Calvin cycle (Mimura et al., 1990). 337

Orthophosphate in the chloroplast stroma functions as a substrate for ATP synthesis. 338

Phosphorous deficiency significantly reduces Pi levels and significantly reduces ATP production in 339

isolated thylakoids (Figure 4C). This was further supported by significant reductions in the rate 340

constant of ATP synthase (Figure 5A) as a response to the low Pi concentration in chloroplasts. 341

These observations confirmed the modulated response of ATP synthase activity to metabolic or 342

physiological conditions, allowing the regulation of light and assimilatory reactions (Strand and 343

Kramer, 2014). The NADP+ levels, acting as a substrate for the production of NADPH, were also 344

significantly reduced by P deficiency (Figure 4A), indicating that a larger fraction of NADP+ 345

remains in the reduced form (NADPH), because it cannot be utilized in the Calvin cycle due to ATP 346

limitation, and because of a higher PSI activity (Figure 7A). This hypothesis was supported by the 347

total NADPH concentration, which was significantly higher for the P-deficient treatment than for 348

the control and P resupply treatments (Figure 4B). 349

The KM for ATP synthase is expected to range between 0.61 mM Pi; therefore, lowering the Pi 350

concentration in the chloroplast stroma to levels near KM is expected to slow down ATP synthesis 351

and increase ΔpH (Takizawa et al., 2008). Assuming a chloroplast volume of 25 μL mg-1

352

chlorophyll (Sharkey and Vanderveer, 1989), the Pi concentrations for chloroplasts extracted after 353

light adaptation correspond to 1.1 and 0.7 mM Pi for the control and P-deficient treatments, 354

respectively, which is in the same range as previous reports using colorimetric assays (Robinson 355

and Giersch, 1987; Sharkey and Vanderveer, 1989) (Figure 4E), and clearly within the range that 356

would affect ATP synthesis. Thus, our results show that ATP synthase activity is very sensitive to 357

changes in the Pi concentration in chloroplasts, and even minor reductions in stromal Pi 358

concentration have a major influence on ATP synthase activity, which strongly reduces proton 359

efflux from the lumen. 360

361

Phosphorus deficiency induces lumen acidification and prevents plastoquinol oxidation 362

The reduced rate constant of ATP synthase under P-deficient conditions limits the export of protons 363

to the chloroplast stroma, thereby markedly acidifying the thylakoid lumen (Figure 5B). As a 364

consequence, the PQH2 oxidation at the Cyt b6f complex was impaired for the P-deficient plants 365

(Table 2), which further decreased the linear electron flow towards PSI (Table 1). This lumen 366

acidification was also reflected by a much faster quenching of the chlorophyll a fluorescence 367

intensity after reaching its maximum (Figure 2A), an increase in qE (Figure 6A), and a higher NPQ 368

(Table 1, Supplementary Figure S5). These observations were further supported by the PSMT decay 369

phase of the extended chlorophyll a fluorescence transient (Supplementary Figure S4). In addition 370

to increased fluorescence quenching, chlorophyll a fluorescence transients of P-deficient plants also 371

lacked the S-step. A previous study of isolated chloroplasts of pea leaves identified a linear 372

relationship between P-S quenching and lumen acidification (Briantais et al., 1979), and a more 373

recent study concludes that formation of the S-step is associated with increased ΔpH (Goltsev et al., 374

2016). These combined data strongly support our hypothesis that P deficiency at physiologically 375

relevant concentrations causes lumen acidification in both light- and dark-adapted plants. 376

A reduction in lumen pH provides the key signal to regulate light capturing via NPQ 377

components (Ruban, 2016), and the present study confirmed the relationship between NPQ and 378

lumen acidification induced by P deficiency (Table 1, Supplementary Figure S5). These adaptive 379

mechanisms enhance the dissipation of excess energy captured by the light-harvesting antenna to 380

protect the photosynthetic apparatus (Stirbet and Govindjee, 2011). The oxygen-evolving complex 381

(OEC) of PSII is particularly affected by lumen acidification (Schlodder and Meyer, 1987). The 382

PSII quantum yield determined from chlorophyll a fluorescence transients of dark-adapted leaves 383



10

was not affected by P deficiency (Figure 2A). However, to determine the influence of ΔpH on PSII 384

quantum yield and ETR(II) in light, we also performed measurements on light-adapted leaves 385

(Table 1, Figure 6B). Here, it is clearly evident that the PSII quantum yield is markedly reduced by 386

P deficiency, but recovers after a subsequent dark-adaption period, which highlights the highly 387

reversible response to P deficiency in plants. 388



11

Conclusion 389

The reversible nature of the disruptions in photosynthesis caused by P deficiency allows us to build 390

a comprehensive biological model summarizing the effects of P deficiency on photosynthesis 391

(Figure 8). Phosphorus is the substrate for ATP synthesis in the chloroplast stroma. When the Pi 392

substrate is lacking due to low P availability (Figure 1, Figure 4D;E;F), ATP synthase activity 393

decreases (Figure 5A), which reduces ATP production in the stroma and CO2 fixation (Figure 4C, 394

Figure 8B; Step 1, 2). Reduced ATP synthase activity reduces the flow of protons from the 395

thylakoid lumen to the chloroplast stroma, which causes lumen acidification (Figure 5B, Figure 8B; 396

Step 3). Lumen acidification triggers energy dissipation via NPQ (Table 1, Supplementary Figure 397

S5), where the major and most rapid component (qE) is responsible for the efficient quenching of 398

fluorescence (Figure 6A, Figure 2A, Supplementary Figure S4), and reduces the PSII quantum yield 399

(Table 1, Figure 6B, Supplementary Figure S5, Figure 8B; Step 4). Acidification of the thylakoid 400

lumen was found to decelerate PQH2 oxidation at the Cyt b6f complex (Table 2, Figure 8B; Step 5), 401

and is likely to represent a bottleneck in overall electron transport from PSII to PSI (Tikhonov, 402

2013; Strand and Kramer, 2014). This causes protonation of the donor side of Cyt b6f and reduces 403

the probability of PQH2 oxidation, ultimately reducing the linear electron flow to PSI (Tikhonov, 404

2014) (Table 1, Figure 6B). Finally, P700+ reduction is either decreased under high light (2,200 405

μmol photons m−2

s−1

, Figure 7B), or increased in steady-state growth light (300 μmol photons m−2

406

s−1

, Figure 7A, Figure 8B; Step 6), which ultimately increases the NADPH levels (Figure 4A, B, 407

Figure 8B; Step 7). Thus, depletion of the I-step phase from the OJIP region of the chlorophyll a 408

fluorescence transient under P deficiency is likely to reflect a restricted PQH2 oxidation due to the 409

proton backlog caused by lumen acidification. 410



12

Materials and methods 411

Plant cultivation and sampling 412

Barley (Hordeum vulgare cv. Quench) plants were cultivated in hydroponics as described 413

previously (Frydenvang et al., 2015). Barley seeds were pre-germinated in vermiculite in a 414

greenhouse with minimum day/night temperatures of 18°C/15°C and a day/night cycle of 16 h/8 h 415

(minimum 300 μmol photons m−2

s−1

light intensity). After 7 days, four seedlings were placed in a 416

lid and transferred to a 4 L hydroponic container and kept at the same climatic conditions 417

throughout the whole experiment. Control plants were supplied with a nutrient solution containing 418

200 µM KH2PO4, 200 µM K2SO4, 300 µM MgSO4·7 H2O, 100 µM NaCl, 300 µM Mg(NO3)2·6 419

H2O, 900 µM Ca(NO3)2·4 H2O, 600 µM KNO3, 50 µM Fe(III)-EDTA-Na, 2.0 µM H3BO3, 0.8 µM 420

Na2MoO4·2 H2O, 0.7 µM ZnCl2, 1.0 µM MnCl2·4 H2O, and 0.8 µM CuSO4·5 H2O. The P-deficient 421

plants were supplied with the same nutrient solution as stated above, but only with 9 µM KH2PO4, 422

throughout the growth period. All nutrients were prepared in Milli-Q water (Milli-Q Element, 423

Millipore, France). The nutrient solutions were changed weekly and aerated using steel medical 424

syringes, and the pH of the solution was maintained at 6.0 ± 0.3 using ultrapure HCl. 425

Four containers holding a total of 16 plants received the full nutrient solution throughout the 426

experiment (control), and 8 containers holding a total of 32 plants received the P-deficient solution. 427

After either 21 or 25 DAP, four P-deficient containers holding a total of 16 plants were resupplied 428

with P corresponding to the control level (200 µM KH2PO4), and the remaining four containers 429

continued to receive the P-deficient solution. All plants were harvested at 28 DAP, either 3 or 7 430

days after P resupply. Each treatment included four hydroponic pots containing four barley plants 431

each (i.e., 16 plants for each treatment). All plants were kept in a dark room the night before 432

harvest, exposed to 1 h of light, and then harvested. One youngest, fully-expanded leaf (YFEL) 433

from each plant was dried and used for elemental analysis, and one YFEL was used directly for 434

determining the NADP+ concentration, and one YFEL was harvested after 8 h of growth conditions 435

for starch determination. The remaining YFELs were harvested 1 h after the onset of light and 436

quickly frozen in liquid nitrogen, and subsequently used to isolate thylakoid membranes. An 437

identical treatment of plants was used entirely for isolating chloroplasts. Chlorophyll a fluorescence 438

was measured before P resupply at 21 DAP and before harvest at 28 DAP, when pulse-amplitude 439

modulation (PAM) measurements were also performed. All analyses were performed with a 440

minimum of four biological replicates. 441

442

Arabidopsis mutants 443 Seeds of Arabidopsis mutants psad1-1 (Ihnatowicz et al., 2004) and psae1-3 (Ihnatowicz et al., 444

2007) and the wild type were sown directly in pots (5.5 cm diameter) containing pre-wetted 445

Pindstrup substrate no. 2 (Pindstrup Mosebrug, DK) in a climate chamber with minimum day/night 446

temperatures of 23°C/18°C and day/night cycles of 8 h/16 h (150 μmol photons m−2

s−1

light 447

intensity). The pots were sealed during the first 7 days to increase humidity, and were watered when 448

needed. Chlorophyll a fluorescence transients were measured after 6 weeks of growth. 449

450

Chlorophyll a fluorescence, P700, and electrochromic band shift 451

Chlorophyll a fluorescence transients (OJIP transients) were obtained from YFELs using a Handy 452

PEA chlorophyll fluorometer (Hansatech Instruments, UK). The YFEL mid-section was dark-453

adapted for at least 25 min before measurements, which were obtained using Hansatech leaf clips, 454

and a short non-actinic light flash was applied to the leaf to adjust the detector gain. Each leaf 455

sample was illuminated with continuous saturating actinic light (3,000 μmol photons m-2

s-1

) from 456

three LEDs, and the fluorescence transients were recorded using a PIN photodiode. The 457



13

fluorescence signal was measured for either 2 or 10 s. To measure the slow PSMT phase, the 458

incident light was 1,000 μmol photons m-2

s-1

and the fluorescence transient was measured for 30 s. 459

All transients were double-normalized between F0 and FM to give the relative variable fluorescence 460

at time t as follows: V(t) = [Fluorescence (t)F0]/(FMF0). 461

Electrochromic band shift (ECS), pulse-amplitude modulated chlorophyll a fluorescence, and 462

P700 measurements were carried out using a Walz Dual-PAM 100 equipped with P515/535, 463

DUAL-DB, and DUAL-E emitter-detector modules. The rate constant of ATP synthase (gH+ s

-1) and 464

PMF partitioning (, pH) was determined on plants that were dark-adapted for a minimum of 1 465

h followed by 1 min of illumination with actinic red light of 339 μmol photons m-2

s-1

. The gH+ 466

parameter was calculated as 1/decay time constant, which was derived from single exponential 467

fittings of the ECS decay signal during an 80 ms dark pulse (Cruz et al., 2005) after 1 min of 468

illumination. PMF (ECST) partitioning to (ECSSS) and pH (ECSINV) was calculated from a 60 469

s dark interval relaxation kinetics (DIRK) of the ECS signal (Cruz et al., 2001). ECST was 470

calculated as the difference between the ECS signal in light and the minimum value of the ECS 471

signal after the light was turned off. Calculation of ECSSS and ECSINV was performed using either 472

the steady-state time point of the ECS signal in darkness, or the time point before the ECS signal 473

decays again due to changes in pigment composition. See Supplementary Figure S8 for calculation 474

of the results presented in Figure 5B. Before each ECS measurement, a saturating 50-μs flash of 475

200,000 μmol photons m−2

s−1

was applied to determine the ECS50μs; subsequently, the ECS50μs 476

amplitude was used to normalize the DIRK ECS signal before calculation of PMF size and 477

partitioning values. Therefore, A550-515 represents the normalized ECS signal to ECS50μs. NPQ 478

and PSII quantum yield were measured using plants that had been dark-adapted for 30 min, 479

illuminated with high light (1,700 μmol photons m−2

s−1

) for 5 min, and then held for 4 min of dark 480

relaxation. qE was calculated as the difference between NPQ after 3 min of illumination and NPQ 481

after 5 min of subsequent dark adaptation. P700 oxidation-reduction kinetics were recorded on 482

plants that had been dark-adapted for a minimum of 1 h, illuminated with far-red light for 30 s, and 483

then saturated with a pulse of actinic red light (20,000 μmol photons m-2

s-1

) for 1 s. ETR(I) was 484

calculated as P700 s-1

according to Strand et al. (2017) by fitting a linear function on the initial 485

decay of the P700 signal upon applying a dark pulse. P700 s-1

was determined on leaves pre-486

illuminated with actinic red light (620 nm; Figure 6C, 7A, 7B, and part of Supplementary Figure 487

S7), or actinic red light and far-red light (730 nm; part of Supplementary Figure S7). State transition 488

was carried out according to Lunde et al. (2000) at 60 mol photons m-2

s-1

; the qS parameter was 489

calculated according to Damkjaer et al. (2009). 490

491

Leaf infiltration with phosphorus and chemical electron inhibitors 492

The YFELs of 28-day-old P-deficient barley plants were cut into 5-cm sections and immersed in 1 493

M KH2PO4 containing 0.2 mL L-1

Tween 20 for 1 h. Then, the leaf sections were removed from the 494

immersion solution and gently wiped to remove excess moisture, placed in a zip bag, and dark-495

adapted for 25 min. As a control, leaves from the same plant treatment were immersed in Milli-Q 496

water containing 0.2 mL L-1

Tween 20. 497

YFELs of 28-day-old control barley plants were infiltrated with 200 µM 3-(3,4–498

dichlorophenyl)-1,1-dimethylurea (DCMU), 900 µM dibromothymoquinone (DBMIB), or 200 µM 499

methyl viologen (MV) as described previously (Schansker et al., 2005). DCMU and DBMIB were 500

solubilized in 1% ethanol. The leaves were cut into 3-cm sections and immersed in the respective 501

solutions for 3 h. Subsequently, the sections were placed in zip bags and dark-adapted for 25 min 502

before recording chlorophyll a fluorescence. Control leaves were treated in the same way without 503

adding the chemical electron inhibitors. 504

505



14

NADP+ and NADPH assay 506

The NADP+ concentration was determined as described previously (Queval and Noctor, 2007), and 507

every step was performed at 4°C. A total of 100 mg of fresh YFELs from each replicated treatment 508

was harvested at 28 DAP and rapidly frozen in liquid nitrogen. Then, 1 mL of ice-cold 0.2 N HCl 509

was added to a mortar with quartz sand, the plant material was thoroughly ground, and centrifuged 510

at 16,000 g for 10 min at 4°C. A 0.2-mL aliquot of the supernatant was incubated in boiling water 511

for 1 min, and then rapidly cooled. The aliquot was neutralized by adding 20 µL of 0.2 M NaH2PO4 512

(pH 5.6), followed by stepwise addition of 0.2 M NaOH to reach a final pH of between 5 and 6. 513

Then, 30 μL of the neutralized supernatant was introduced to a 96-well plate, in which each well 514

contained 0.1 mL of 0.1 M HEPES (pH 7.5) and 2 mM EDTA, 20 µL of 1.2 mM 515

dichlorophenolindophenol (DCPIP), 10 µL of 20 mM phenazine methosulfate (PMS), 10 µL of 10 516

mM glucose-6-phosphate (G6P), and 30 µL Milli-Q water. NADP+ concentrations ranging from 517

0100 pmol were used as standards. The reaction was started by adding 10 µL glucose-6-phosphate 518

dehydrogenase (200 U mL-1

), the plate was rapidly swirled and placed on an EON microplate 519

spectrophotometer (BioTek Instruments, USA), and the absorbance at 600 nm was measured every 520

23 s for 5 min. The rates during the first 2 min were used to determine the final NADP+ 521

concentration according to the relevant standards and blank correction. 522

The NADPH concentration was determined using a NADP/NADPH Quantification Kit (Sigma-523

Aldrich, USA, catalog number MAK038), following the protocol from the manufacturer. An EON 524

microplate spectrophotometer (BioTek Instruments, USA) was used to measure the absorbance at 525

450 nm after 2 h of incubation. 526

527

Isolation of thylakoid membranes 528

All extractions were performed at 4°C under dim-green light conditions to maintain thylakoid 529

integrity. Frozen YFELs were homogenized in 200 mL of buffer solution containing 0.4 M sucrose, 530

10 mM NaCl, 5 mM MgCl2, 20 mM Tricine (pH 7.9), 10 mM L-ascorbate, and 10 mM NaF using a 531

laboratory blender (Waring Laboratory LB20E, Connecticut, USA). The homogenate was filtered 532

through a double layer of Miracloth (pore size 22–25 mm). The extracts were centrifuged for 10 533

min at 6,000 g, the supernatant was discarded, and the pellet was resuspended in 5 mM Tricine (pH 534

7.9) and 10 mM NaF. The washed thylakoids were pelleted by centrifugation for 10 min at 11,200 g 535

and re-suspended in a storage solution containing 0.4 M sucrose, 10 mM NaCl, 5 mM MgCl2, 20 536

mM Tricine (pH 7.9), 10 mM NaF, and 20% glycerol. The samples were immediately frozen in 537

liquid nitrogen and stored at 80°C. 538

539

Determination of protein and chlorophyll content in thylakoid membranes 540

The protein content in the isolated thylakoid membranes was determined using the Pierce BCA 541

Protein Assay Kit (ThermoFisher Scientific, USA), and an EON microplate spectrophotometer 542

(BioTek Instruments, USA) was used to measure the absorbance at 562 nm. To determine the 543

chlorophyll concentration, 5 μL of the isolated thylakoid membrane was diluted in 995 μL of ice-544

cold 80% acetone, incubated on ice for 15 min, and centrifuged for 2 min at 10,000 g in a tabletop 545

microcentrifuge (Eppendorf Minispin Plus, USA) to pellet proteins. The absorbance at 647 and 664 546

nm was measured using a Genesys 10S UV-VIS spectrophotometer (ThermoFisher Scientific, 547

USA), and the total chlorophyll concentration (μg/mL) was calculated as (17.76×A647)+(7.34×A664) 548

multiplied by the dilution factor (Porra et al., 1989). 549

550

Chloroplast isolation 551

Plants were either dark-adapted for 10 h or light-adapted at growth conditions for 4 h prior to 552

isolation. All extractions were performed at 4°C under dim-green light conditions. All YFELs from 553



15

each replicate were cut into 34 cm sections and placed in a blender containing 200 mL ice-cold HS 554

buffer (50 mM HEPES and 330 mM sorbitol, adjusted to pH 8 with KOH pellets), and rapidly 555

blended with three quick bursts. The homogenate was filtered through a double layer of Miracloth 556

(pore size 22–25 mm) and centrifuged at 3,300 g for 2 min in a swing rotor (Heraeus Megafuge 557

16R, ThermoFisher Scientific, USA) with slow acceleration and without brakes for deceleration. 558

The supernatant was carefully discarded and the tubes were rolled on ice to loosen the pellets. Then, 559

1 mL of HS buffer was added and the suspension was layered onto a pre-cooled Percoll pad 560

containing 2 mL of 5x HS buffer, 3.5 mL Percoll, and 4.5 mL Milli-Q water, and centrifuged at 561

1,400 g for 8 min in a swing rotor. The green middle layer (containing thylakoids and broken 562

chloroplasts) and the Percoll were carefully removed, leaving the pelleted intact chloroplasts. The 563

pellet was suspended in 10 mL of HS buffer and centrifuged at 3,000 g for 2 min in a swing rotor. 564

The supernatant was discarded and the pellet was suspended in 700 μL HS buffer and stored at 565

80oC until use. 566

567

Determination of chlorophyll content in isolated chloroplasts 568

The chlorophyll concentration in the isolated chloroplasts was determined by adding 10 µL 569

chloroplasts to 990 µL ice-cold 80% acetone, mixing the solution, and centrifuging for 30 s at 570

10,000 g in a tabletop microcentrifuge (Eppendorf Minispin Plus, USA) to pellet the proteins. The 571

absorbance at 652 nm was measured using a Genesys 10S UV-VIS spectrophotometer 572

(ThermoFisher Scientific, USA). The chlorophyll (µg/µL) concentration was determined using the 573

following equation: (A652×5.6) (Robinson and Mant, 2002). 574

575

Determination of the plastoquinone pool redox state 576

A non-invasive assay of the plastoquinone pool redox state was performed following the protocol 577

from Tóth et al. (2007). To obtain fully reduced PQ-pools, OJIP transients were measured at 578

saturating actinic light (3,000 μmol photons m-2

s-1

) as described above. To obtain fully oxidized 579

PQ-pools, leaves were pre-illuminated with far-red light (200 μmol photons m−2

s−1

) for 10 s, and a 580

second OJIP transient was measured immediately after. From the first OJIP transient, the FJ 581

(fluorescence intensity after 3 ms – J-step) and FM value was extracted, whereas the FJ-ox 582

(representing the fully oxidized PQ-pool at 3 ms) was extracted from the far-red light treatment. 583

The fraction of reduced PQ was calculated using the following equation: (FJ-FJ-ox)/(FM-FJ-ox), where 584

0 and 1 represent a fully oxidized and fully reduced PQ-pool, respectively. 585

586

ATP assay 587

ATP concentrations were determined in thylakoid membranes as described previously (Grennan 588

and Ort, 2011). A thylakoid membrane aliquot containing 20 μg of chlorophyll was resuspended in 589

1 mL buffer containing 500 mM Tricine-NaOH (pH 8.0), 500 mM NaCl, 5 mM MgCl2, 0.05 mM 590

phenazine methosulfate (PMS), 2 mM K2HPO4 (pH 7.0), 1 mM ADP (ATP-free), and 0.1 mM 591

diadenosine pentaphosphate. The reaction was carried out with incident light at 300 μmol m-2

s-1

for 592

2 min at room temperature. Then, the light was switched off and the reaction was stopped by adding 593

trichloroacetic acid to a final volume of 0.5% (w/v). The samples were centrifuged at 11,200 g for 5 594

min at room temperature. The supernatant was assayed for ATP concentration by measuring 595

chemiluminescence using a ChemiDoc Touch Imaging System (Bio-Rad, USA). A 100-μL aliquot 596

of the supernatant was added to a 96-well plate, and 100 μL of a second buffer containing 25 mM 597

Tris-acetate (pH 7.75), 2 mM EDTA, 50 mM dithiothreitol (DTT), 0.02 mM D-luciferin, 1.5 598

mg/mL bovine serum albumin (BSA), 20 mM magnesium acetate, and 0.3 μg/mL luciferase was 599

quickly added to each well. The chemiluminescence was measured during a 20-min period, and the 600



16

signal was integrated using Image Lab software (version 5.2.1; Bio-Rad, USA). The same reaction 601

mix was used to determine ATP standards dissolved in 25 mM Tris-acetate (pH 7.75). 602

603

Orthophosphate quantification 604

Orthophosphate was quantified by high-performance liquid chromatography (HPLC) as described 605

previously (Hawkesford et al., 2013). A total of 100 mg of dried YFEL material was added to 1.5 606

mL of Milli-Q water and heated in a heating block at 80°C for 4 h with frequent shaking. To 607

quantify orthophosphate in isolated chloroplasts, a chloroplast preparation containing 20 μg of 608

chlorophyll in 200 μl HS buffer was directly heated in a heating block at 80°C for 4 h. The samples 609

were allowed to cool and then centrifuged at room temperature at 13,000 g for 20 min. The 610

supernatant was transferred to a 2 mL Eppendorf tube and placed at 20°C overnight. After 611

thawing, the sample was centrifuged as before, and the supernatant was filtered using a 0.22-μm 612

centrifuge tube filter (Spin-X, Costar, USA) at 2,000 g for 20 min. This sample was injected onto 613

the HPLC column. 614

The samples were analysed on the HPLC Dionex ICS-2100 Anion (ThermoFisher Scientific, 615

USA) column using the Dionex AS-AP autosampler, Dionex EGC III KOH eluent generator, AERS 616

2 mm suppressor, and DS6 heated conductivity cell. Anions were separated on a Dionex IonPac 617

AS11-HC RFIC analytical column (2x250 mm) with a Dionex IonPac AG11-HC RFIC guard (2x50 618

mm) column in front, with 0.38 mL min-1

isocratic flow of 25 mM hydroxide for 15 min. The 619

suppressor was set to 24 mA, and 25 µL was injected per sample. The standard curve was generated 620

with five concentrations of Dionex Combined Seven Anion Standard I (ThermoFisher Scientific, 621

USA) from 0.15–2.0 mg L-1

in HS buffer. Chromeleon 7.2 SR4 software was used for instrument 622

control and data processing. 623

624

Starch quantification 625

The starch concentration was determined as described previously (Smith and Zeeman, 2006). 626

Frozen YFELs were ground to a fine powder, 5 mL of 80% ethanol (v/v) was added, and the sample 627

was placed in a boiling water bath for 3 min. The samples were centrifuged at 3,000 g for 10 min at 628

room temperature, and the supernatant was discarded. The ethanol extraction was repeated another 629

two times, and the ethanol was allowed to evaporate from the final pellet. The pellet was transferred 630

to a mortar, homogenized to a smooth consistency, and transferred to a Falcon tube along with 5 631

mL of Milli-Q water that was used to wash the mortar. Then, 0.5 mL of the homogenate was added 632

to each of four Eppendorf tubes and heated at 100°C for 10 min. The samples were allowed to reach 633

room temperature and then 0.5 mL of 200 mM sodium acetate (pH 5.5) was added. In another tube, 634

6 U of α-amyloglucosidase and 0.5 U of α-amylase were dissolved in buffer containing 0.05 mM 635

Tris base, 0.15 mM NaCl, and 0.1% Tween 20 (pH adjusted to 7.6 using HCl); 1.2 mL of this 636

enzyme preparation was added to two of the prepared Eppendorf tubes. The other two Eppendorf 637

tubes were used as controls, which received 1.2 mL of buffer without the enzymes. The samples 638

were incubated at 37°C for 4 h and centrifuged at 10,000 g for 5 min at room temperature. The 639

supernatant was assayed for glucose using a Glucose (HK) Assay Kit (Sigma-Aldrich, USA). The 640

assay reagents were mixed and the reactions were incubated for 15 min at room temperature before 641

measuring the absorbance at 340 nm using a Genesys 10S UV-VIS spectrophotometer 642

(ThermoFisher Scientific, USA). 643

644

Immunoblot analysis 645

Thylakoid samples (containing 5 μg protein) were subjected to SDS-PAGE using 12% Criterion 646

TGX Stain-Free precast gels (Bio-Rad, USA) and Tris/Glycine/SDS running buffer (Bio-Rad, 647

USA) at a constant voltage of 250 V for 30 min. The proteins were then transferred to a 0.2 mm 648



17

PVDF membrane using the Trans-Blot Turbo Transfer System (Bio-Rad, USA) according to the 649

manufacturer’s instructions. Subsequently, the membrane was blocked for 1 h in 5% (w/v) skimmed 650

milk in PBS-T buffer, and incubated overnight in the primary antibody. All primary antibodies 651

(FNR, ferredoxin (FDX1), PsaA, PsaF, Cyt f, D1, and CP43) were obtained from Agrisera (AB, 652

Sweden). The blot was washed three times for 5 min in PBS-T buffer and then incubated with a 653

swine anti-rabbit HRP-conjugated secondary antibody (1:5,000 dilution in PBS-T; Pierce, USA) for 654

1 h. The blot was washed three times for 5 min in PBS-T buffer and the secondary antibody was 655

detected using Clarity Western ECL chemiluminescent substrate (Bio-Rad, USA) and the 656

ChemiDoc Touch Imaging System (Bio-Rad, USA). The protein bands were detected and 657

quantified using Image Lab software (version 5.2.1; Bio-Rad, USA). 658

659

Transmission electron microscopy 660

The YFELs from three replicated treatments in both dark and light conditions were used for 661

transmission electron microscopy analysis. Leaf discs (12 mm2) were fixed in Karnovsky’s 662

solution (4% paraformaldehyde, 5% glutaraldehyde, and 0.1 M sodium cacodylate buffer, pH 7.3) 663

for 4 h and washed three times with buffer (0.1 M sodium cacodylate buffer, pH 7.3). Samples were 664

post-fixed with 1% OsO4 overnight at 4°C. The samples were washed twice with buffer and water, 665

and subsequently dehydrated with a graded acetone series. The leaf samples were embedded in 666

Spurr’s low-viscosity resin. Ultrathin sections of 60 nm were cut with a diamond knife using a 667

Leica EM-UC7 ultra-microtome and mounted on Pioloform-coated copper grids. The samples were 668

contrasted with 1% uranyl acetate and lead citrate, and viewed using a Philips CM100 transmission 669

electron microscope at an acceleration voltage of 80 kV. The images were captured using a high-670

resolution Morada digital camera system. 671

672

Elemental analyses 673

Leaf element concentrations were determined using inductively-coupled plasma-optical emission 674

spectroscopy (ICP-OES) (5100, Agilent Technologies, USA) equipped with a Meinhard nebulizer 675

and a cyclonic spray chamber. The YFELs were oven-dried at 50°C until complete dryness and 676

digested with ultra-pure acids (70% HNO3 and 30% H2O2) at 240°C and 200 bars for 15 min in a 677

pressurized microwave oven (Ultrawave, Milestone Inc., Italy). Certified reference material 678

[NIST1515, apple (Malus ssp.) leaf, National Institute of Standards and Technology, USA] was 679

included to evaluate data quality. Data were processed using Agilent ICP Expert software. 680

681

Data analyses 682

Statistical analysis was performed using GraphPad Prism 6.0 for Windows. Each mean was 683

compared using one-way ANOVA analysis with Tukey’s multiple comparison test. Samples were 684

considered as significantly different at P<0.05. 685



18

Supplemental Data 686 The following supplemental materials are available. 687

Supplemental Figure S1. Appearance of barley plants cultivated in hydroponics. 688

Supplementary Figure S2. Transmission electron microscopy of barley leaves. 689

Supplementary Figure S3. Immunoblot analysis of photosynthetic proteins in barley leaves. 690

Supplementary Figure S4. OJIPSMT transients of the youngest, fully-expanded leaves of barley 691

plants. 692

Supplementary Figure S5. Non-photochemical quenching and photosystem II quantum yield in 693

barley leaves. 694

Supplementary Figure S6. P700+ reduction kinetics in barley plants. 695

Supplementary Figure S7. P700+ reduction kinetics in barley under low light. 696

Supplementary Figure S8. Examples of analysis of raw data leading to the data presented in 697

Figure 5B. 698

Supplementary Table S1. Element concentrations in the youngest, fully-expanded leaves. 699

Supplementary Table S2. Quantification of immunoblots of thylakoid protein extracts. 700

Supplementary Table S3. State transition parameters and electron transfer rates in low light. 701

702

703

Acknowledgments 704

We thank Lena Byrgesen and Thomas H. Hansen for assistance with the inductively-coupled 705

plasma-optical emission spectroscopy analyses, and Birgit Andersen for assistance with the HPLC 706

measurements. Transmission electron microscopy was performed at the Center of Advanced 707

Bioimaging (CAB), University of Copenhagen, Denmark. 708



19

Table 1. Photosynthetic parameters measured under steady-state growth light conditions. The plants were 709 light-adapted in growth light (300 μmol photons m−2 s−1) for a minimum of eight hours and measured 710 afterwards using the Leaf Photosynthesis MultispeQ V1.0 protocol with the MultispeQ from PhotosynQ. The 711 results are means ± SEM (n=4-5, each with >4 technical replicates), and different letters represent 712 statistically significant changes (P<0.05) using a one-way ANOVA analysis and Tukey’s multiple 713 comparison test. 714

Treatment ɸ(II) ɸ(NO) ɸ(NPQ) LEF qP NPQt

Control 0.53a ± 0.01 0.31a ± 0.01 0.16a ± 0.01 79.48a ± 3.66 0.69a ± 0.02 0.54a ± 0.02

P deficient 0.30b ± 0.02 0.13b ± 0.01 0.57b ± 0.03 45.22b ± 4.29 0.60b ± 0.02 5.11b ± 0.69

P resupply 0.47a ± 0.02 0.33a ± 0.02 0.19a ± 0.01 77.39a ± 3.09 0.63ab ± 0.03 0.60a ± 0.03

715

Table 2. The plastoquinone pool redox state in barley leaves. Estimation of the fraction of reduced PQ was 716 determined using OJIP transients. The results are means ± SEM (n=4, each with 4 technical replicates), and 717 different letters represent statistically significant changes (P<0.05) using a one-way ANOVA analysis and 718 Tukey’s multiple comparison test. 719

Treatment Fraction of PQH2

Control 0.27a ± 0.01

P deficient 0.36b ± 0.02

P resupply 0.28a ± 0.01

720

721



20

Figure 1. Leaf phosphorus concentrations with corresponding photos of the youngest fully-expanded barley 722 leaves. Control, P-deficient, and P-resupplied barley plants were cultivated in hydroponics. Phosphorus was 723 resupplied to the nutrient solution 21 days after planting (DAP), and each photograph was taken before 724 harvest seven days later (28 DAP). The P concentrations are mean values in leaf dry matter ± SEM (n=4, 725 each with 4 technical replicates), and different letters represent statistically significant changes (P<0.05) 726 using a one-way ANOVA analysis and Tukey’s multiple comparison test. 727

728

Figure 2. OJIP transients recorded from the youngest, fully-expanded barley leaves. A, main plot: Transients 729 were recorded just before P resupply at 21 days after planting (DAP). Inset: Transients were recorded seven 730 days after P resupply at 28 DAP. The slope of the quenching curve was calculated between the two dashed 731 vertical lines (between 2 and 10 s). B, transients recorded for P-deficient leaves immersed in Mili-Q water 732 (P-deficient) or P solution (P-resupply) for 60 min. All transients were averaged (a, n=5; b, n=4, each with 733 >4 technical replicates) and doubled-normalized between F0 and FM. 734

735

Figure 3. OJIP transients recorded from barley leaves infiltrated with electron inhibitors or from Arabidopsis 736 PSI mutants. A, effects of DCMU, DBMIB, and MV inhibitors on OJIP transients in the YFELs of 28-day-737 old healthy barley plants (control) cultivated in hydroponics. B, OJIP transients from 6-week-old 738 Arabidopsis mutants psad1-1 and psae1-3 and the corresponding wild type cultivated in soil. The transients 739 were averaged (a, n=4; b, n=5, each with 4 technical replicates) and double-normalized between F0 and FM. 740

741

Figure 4. Concentrations of NADP+, NADPH, ATP, orthophosphate (PO43), and starch in the youngest, 742

fully-expanded barley leaves. A, concentrations of NADP+ in leaf tissue. B, concentrations of NADPH in 743 leaf tissue. C, concentrations of ATP in light-exposed thylakoids. D, concentrations of PO4

3 in leaf tissue. E, 744 concentrations of PO4

3 in chloroplasts isolated after a 10 h dark period. F, concentrations of PO43 in 745

chloroplasts isolated after a 4 h light period. G, concentration of starch in leaf tissue. The results are means ± 746 SEM (n=4, each with >4 technical replicates), and different letters represent statistically significant changes 747 (P<0.05) using a one-way ANOVA analysis and Tukey’s multiple comparison test. 748

749

Figure 5. ATP synthase activity and proton motive force partitioning in barley. A, relative thylakoid proton 750 conductivity, which reflects activity of ATP synthase. B, relative pmf partitioning in control, P-deficient, and 751 P-resupplied barley plants. Values are means ± SEM (n=5, each with >4 technical replicates), and different 752 letters represent statistically significant changes (P<0.05) using a one-way ANOVA analysis and Tukey’s 753 multiple comparison test. Greek letters indicate statistical differences in ΔpH, and Roman letters indicate 754 differences in ΔΨ. 755

756

Figure 6. The energy dependent quenching component (qE) and electron transfer rates (ETR) at different 757 light intensities in barley. Light-adapted barley plants were exposed to increasing light intensities (red actinic 758 light with a wavelength of 620 nm), starting at growth light. A, the qE component of NPQ. B, electron 759 transfer rates of PSII (ETR(II)). C, electron transfer rates of PSI (ETR(I)). Values are means ± SEM (n=4-5, 760 each with >4 technical replicates). 761

762

Figure 7. P700+ reduction kinetics in barley. A, P700+ reduction in growth light conditions. B, P700+ 763

reduction in high light conditions. Plants were light adapted for >2 h prior measurements, then pre-764 illuminated with red actinic light (620 nm) for 3 min, followed by a 10 ms dark pulse. The plotted transients 765 are averaged (n=5, each with >4 technical replicates). 766

767

Figure 8. Photosynthetic regulation in response to phosphorus deficiency at growth light conditions. A, 768 photosynthetic electron flow under sufficient P conditions. B, feedback mechanisms responsible for reduced 769



21

electron flow from PSII to PSI under P deficiency conditions. See text for further explanation of the cascade 770 of events highlighted in step 1-7. 771 772



22

References 773

Antal TK, Osipov V, Matorin DN, Rubin AB (2011) Membrane potential is involved in regulation of 774

photosynthetic reactions in the marine diatom Thalassiosira weissflogii. J Photochem 775

Photobiol B Biol 102: 169–173 776

Baker A, Ceasar SA, Palmer AJ, Paterson JB, Qi W, Muench SP, Baldwin SA (2015) Replace, reuse, 777

recycle: Improving the sustainable use of phosphorus by plants. J Exp Bot 66: 3523–3540 778

Belatik A, Joly D, Hotchandani S, Carpentier R (2013) Re-evaluation of the side effects of 779

cytochrome b6f inhibitor dibromothymoquinone on photosystem II excitation and electron 780

transfer. Photosynth Res 117: 489–496 781

Briantais JM, Vernotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of 782

chlorophyll a fluorescence in isolated chloroplasts. BBA - Bioenerg 548: 128–138 783

Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for 784

thought. Glob Environ Chang 19: 292–305 785

Cordell D, White S (2015) Tracking phosphorus security: indicators of phosphorus vulnerability in 786

the global food system. Food Secur 7: 337–350 787

Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light 788

reactions of photosynthesis for energy production and photoprotection. J Exp Bot 56: 395–789

406 790

Cruz JA, Sacksteder CA, Kanazawa A, Kramer DM (2001) Contribution of electric field (∆ψ) to 791

steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf 792

parsing into ∆ψ and ∆pH by ionic strength. Biochemistry 40: 1226–1237 793

Damkjaer JT, Kereiche S, Johnson MP, Kovacs L, Kiss AZ, Boekema EJ, Ruban A V., Horton P, 794

Jansson S (2009) The photosystem II light-harvesting protein lhcb3 affects the macrostructure 795

of photosystem II and the rate of state transitions in arabidopsis. Plant Cell 21: 3245–3256 796

Duysens LNM, Sweers HE (1963) Mechanism of two photochemical reactions in algae as studied by 797

means of fluorescence. Stud microalgae Photosynth Bact 353–372 798

Franck F, Juneau P, Popovic R (2002) Resolution of the Photosystem I and Photosystem II 799

contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochim 800

Biophys Acta - Bioenerg 1556: 239–246 801

Frydenvang J, van Maarschalkerweerd M, Carstensen A, Mundus S, Schmidt SB, Pedas PR, Laursen 802

KH, Schjoerring JK, Husted S (2015) Sensitive Detection of Phosphorus Deficiency in Plants 803

Using Chlorophyll a Fluorescence. Plant Physiol 169: 353–61 804

Gilbert N (2009) The disappearing nutrient. Nature 461: 716–718 805

Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) 806

Variable chlorophyll fluorescence and its use for assessing physiological condition of plant 807

photosynthetic apparatus. Russ J Plant Physiol 63: 869–893 808

Grennan AK, Ort DR (2011) Measurement of chloroplast ATP synthesis activity in arabidopsis. In PR 809

Jarvis, ed, Chloroplast Res. Arab. - Metod. Protoc. vol II. Humana Press, pp 343–355 810

Guo B, Jin Y, Wussler C, Blancaflor E, Motes C, Versaw W (2008) Functional analysis of the 811

Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol 177: 889–898 812

Hammond JP, White PJ (2008) Sucrose transport in the phloem: Integrating root responses to 813

phosphorus starvation. J Exp Bot 59: 93–109 814

Hawkesford M, Parmar S, Buchner P (2013) Mineral composition analysis: Measuring anion uptake 815

and anion concentrations in plant tissues. In JM Walker, ed, Plant Miner. Nutr. Humana Press, 816



23

York, UK, pp 109–119 817

Heldt HW, Chon CJ, Maronde D, Herold A, Stankovic ZS, Walker DA, Kraminer A, Kirk MR, Heber U 818

(1977) Role of orthophosphate and other factors in the regulation of starch formation in 819

leaves and isolated chloroplasts. Plant Physiol 59: 1146–1155 820

Ihnatowicz A, Pesaresi P, Leister D (2007) The E subunit of photosystem I is not essential for linear 821

electron flow and photoautotrophic growth in Arabidopsis thaliana. Planta 226: 889–895 822

Ihnatowicz A, Pesaresi P, Varotto C, Richly E, Schneider A, Jahns P, Salamini F, Leister D (2004) 823

Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, 824

photosystem I stability and expression of nuclear genes for chloroplast functions. plant J 37: 825

839–852 826

Karlsson PM, Herdean A, Adolfsson L, Beebo A, Nziengui H, Irigoyen S, Ünnep R, Zsiros O, Garab G, 827

Aronsson H, et al (2015) The Arabidopsis thylakoid transporter PHT4;1 influences phosphate 828

availability for ATP synthesis and plant growth. plant J 84: 99–110 829

Lauer MJ, Pallardy SG, Blevins DG, Randall DD (1989) Whole leaf carbon exchange characteristics 830

of phosphate deficient soybeans (Glycine max L.). Plant Physiol 91: 848–854 831

Lavorel J, Etienne AL (1977) In vivo chlorophyll fluorescence. Prim Process Photosynth 2: 203–268 832

Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller H V, Scheller H V. (2000) The PSI-H subunit of 833

photosystem I is essential for state transitions in plant photosynthesis. Nature 408: 613–5 834

MacDonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances 835

across the world’s croplands. Proc Natl Acad Sci U S A 108: 3086–91 836

Mimura T, Dietz K-J, Kaiser W, Schramm MJ, Kaiser G, Heber U (1990) Phosphate transport across 837

biomembranes and cytosolic phosphate homeostasis in barley leaves. Planta 180: 139–146 838

Młodzińska E, Zboińska M (2016) Phosphate Uptake and Allocation - A Closer Look at Arabidopsis 839

thaliana L. and Oryza sativa L. Front Plant Sci 7: 1198 840

Muneer S, Jeong BR (2015) Proteomic analysis provides new insights in phosphorus homeostasis 841

subjected to pi (inorganic phosphate) starvation in tomato plants (Solanum lycopersicum L.). 842

PLoS One 10: 1–18 843

Müller P, Li X, Niyogi KK (2001) Update on photosynthesis non-photochemical quenching. A 844

response to excess light energy. Plant Physiol 125: 1558–1566 845

Pavón LR, Lundh F, Lundin B, Mishra A, Persson BL, Spetea C (2008) Arabidopsis ANTR1 is a 846

thylakoid Na+-dependent phosphate transporter: Functional characterization in Escherichia 847

coli. J Biol Chem 283: 13520–13527 848

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients 849

and simultaneous equations for assaying chlorophylls a and b extracted with four different 850

solvents: verification of the concentration of chlorophyll standards by atomic absorption 851

spectroscopy. Biochim Biophys Acta 975: 384–394 852

Queval G, Noctor G (2007) A plate reader method for the measurement of NAD, NADP, 853

glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis 854

rosette development. Anal Biochem 363: 58–69 855

Ramaekers L, Remans R, Rao IM, Blair MW, Vanderleyden J (2010) Strategies for improving 856

phosphorus acquisition efficiency of crop plants. F Crop Res 117: 169–176 857

Rao IM, Terry N (1995) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar 858

beet (IV. changes with time following increased supply of phosphate to low-phosphate 859

plants). Plant Physiol 107: 1313–1321 860

Reich PB, Oleksyn J, Wright IJ (2009) Leaf phosphorus influences the photosynthesis-nitrogen 861



24

relation: A cross-biome analysis of 314 species. Oecologia 160: 207–212 862

Reuter DJ, Robinson JB (1997) Plant analysis: An interpretation manual, 2nd ed. CSIRO publishing, 863

Collingwood, Australia 864

Robinson C, Mant A (2002) Molecular plant biology - A practical approach. Oxford Universiy Press 865

Robinson SP, Giersch C (1987) Inorganic phosphate concentration in the stroma of isolated 866

chloroplasts and its influence on photosynthesis. Aust J Pant Physiol 14: 451–62 867

Ruban A V (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and 868

effectiveness in protecting plants from photodamage. Plant Physiol 170: 1903–1916 869

Rychter AM, Rao IM (2005) Role of phosphorus in photosynthetic carbon metabolism. In M 870

Pessarakli, ed, Handb. Photosynth., 2nd ed. CRC Press, pp 123–148 871

Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of 872

pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim 873

Biophys Acta - Bioenerg 1706: 250–261 874

Schlodder E, Meyer B (1987) pH dependence of oxygen evolution and reduction kinetics of 875

photooxidized chlorophyll aII (P-680) in photosystem II particles from Synechococcus sp. 876

Biochim Biophys Acta 890: 23–31 877

Sharkey TD, Vanderveer PJ (1989) Stromal phosphate concentration is low during feedback limited 878

photosynthesis. Plant Physiol 91: 679–684 879

Smith AM, Zeeman SC (2006) Quantification of starch in plant tissues. Nat Protoc 1: 1342–1345 880

Srivastava A, Strasser RJ, Govindjee (1995) Polyphasic rise of chlorophyll a fluorescence in 881

herbicide-resistant D1 mutants of Chlamydomonas reinardtii. Photosynth Res 43: 131–141 882

Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the 883

thermal phase, the J-I-P rise. Photosynth Res 113: 15–61 884

Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence 885

induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient. J 886

Photochem Photobiol B Biol 104: 236–257 887

Stirbet A, Riznichenko G, Rubin A, Govindjee (2014) Modeling chlorophyll a fluorescence transient: 888

relation to photosynthesis. Biochemistry 79: 291–323 889

Strand DD, Fisher N, Kramer DM (2017) The higher plant plastid NAD(P)H dehydrogenase-like 890

complex (NDH) is a high efficiency proton pump that increases ATP production by cyclic 891

electron flow. J Biol Chem 292: 11850–11860 892

Strand DD, Kramer DM (2014) Control of non-photochemical exciton quenching by the proton 893

circuit of photosynthesis. In B Demmig-Adams, G Garab, W Adams, Govindjee, eds, Non-894

photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, 895

pp 387–408 896

Strasser RJ, Govindjee (1992) The Fo and the O-J-I-P Fluorescence Rise in Higher Plants and Algae. 897

In JH Argyroudi-Akoyunoglou, ed, Regul. Chloroplast Biog. Springer US, Boston, MA, pp 423–898

426 899

Takizawa K, Kanazawa A, Kramer DM (2008) Depletion of stromal Pi induces high “energy-900

dependent” antenna exciton quenching (qE) by decreasing proton conductivity at CFo-CF1 901

ATP synthase. Plant Cell Environ 31: 235–243 902

Tietz S, Hall CC, Cruz JA, Kramer DM (2017) NPQ(T): a chlorophyll fluorescence parameter for rapid 903

estimation and imaging of non-photochemical quenching of excitons in photosystem-II-904

associated antenna complexes. Plant Cell Environ 40: 1243–1255 905

Tikhonov AN (2013) pH-Dependent regulation of electron transport and ATP synthesis in 906



25

chloroplasts. Photophysiology 116: 511–534 907

Tikhonov AN (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron 908

transport pathways. Plant Physiol Biochem 81: 163–183 909

Tóth SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox 910

state based on the OJIP-transient. Photosynth Res 93: 193–203 911

Vredenberg WJ (2004) System analysis and photoelectrochemical control of chlorophyll 912

fluorescence in terms of trapping models of photosystem II: a challenging view. Chlorophyll a 913

Fluoresc. Springer, pp 133–172 914

Walan P, Davidsson S, Johansson S, Höök M (2014) Phosphate rock production and depletion: 915

regional disaggregated modeling and global implications. Resour Conserv Recycl 93: 178–187 916

Yan N, Zhang YL, Xue HM, Zhang XH, Wang ZD, Shi LY, Guo DP (2015) Changes in plant growth and 917

photosynthetic performance of Zizania latifolia exposed to different phosphorus 918

concentrations under hydroponic condition. Photosynthetica 53: 630–635 919

Yin L, Vener A V, Spetea C (2015) The membrane proteome of stroma thylakoids from Arabidopsis 920

thaliana studied by successive in-solution and in-gel digestion. Physiol Plant 154: 433–446 921

Zhang K, Liu H, Tao P, Chen H (2014) Comparative proteomic analyses provide new insights into 922

low phosphorus stress responses in maize leaves. PLoS One 9: 1–16 923

924



1

Figure 1. Leaf phosphorus concentrations with corresponding photos of the youngest fully-expanded barley leaves. Control, P-deficient, and P-resupplied barley plants were cultivated in hydroponics. Phosphorus was resupplied to the nutrient solution 21 days after planting (DAP), and each photograph was taken before harvest seven days later (28 DAP). The P concentrations are mean values in leaf dry matter ± SEM (n=4, each with 4 technical replicates), and different letters represent statistically significant changes (P<0.05) using a one-way ANOVA analysis and Tukey’s multiple comparison test.



1

Figure 2. OJIP transients recorded from the youngest, fully-expanded barley leaves. A, main plot: Transients were recorded just before P resupply at 21 days after planting (DAP). Inset: Transients were recorded seven days after P resupply at 28 DAP. The slope of the quenching curve was calculated between the two dashed vertical lines (between 2 and 10 s). B, transients recorded for P-deficient leaves immersed in Mili-Q water (P-deficient) or P solution (P-resupply) for 60 min. All transients were averaged (a, n=5; b, n=4, each with >4 technical replicates) and doubled-normalized between F0 and FM.



1

Figure 3. OJIP transients recorded from barley leaves infiltrated with electron inhibitors or from Arabidopsis PSI mutants. A, effects of DCMU, DBMIB, and MV inhibitors on OJIP transients in the YFELs of 28-day-old healthy barley plants (control) cultivated in hydroponics. B, OJIP transients from 6-week-old Arabidopsis mutants psad1-1 and psae1-3 and the corresponding wild type cultivated in soil. The transients were averaged (a, n=4; b, n=5, each with 4 technical replicates) and double-normalized between F0 and FM.



1

Figure 4. Concentrations of NADP+, NADPH, ATP, orthophosphate (PO43), and starch in the youngest, fully-

expanded barley leaves. A, concentrations of NADP+ in leaf tissue. B, concentrations of NADPH in leaf

tissue. C, concentrations of ATP in light-exposed thylakoids. D, concentrations of PO43 in leaf tissue. E,

concentrations of PO43 in chloroplasts isolated after a 10 h dark period. F, concentrations of PO4

3 in chloroplasts isolated after a 4 h light period. G, concentration of starch in leaf tissue. The results are means ± SEM (n=4, each with >4 technical replicates), and different letters represent statistically significant changes (P<0.05) using a one-way ANOVA analysis and Tukey’s multiple comparison test.



1

Figure 5. ATP synthase activity and proton motive force partitioning in barley. A, relative thylakoid proton conductivity, which reflects activity of ATP synthase. B, relative pmf partitioning in control, P-deficient, and P-resupplied barley plants. Values are means ± SEM (n=5, each with >4 technical replicates), and different letters represent statistically significant changes (P<0.05) using a one-way ANOVA analysis and Tukey’s multiple comparison test. Greek letters indicate statistical differences in ΔpH, and Roman letters indicate differences in ΔΨ.



1

Figure 6. The energy dependent quenching component (qE) and electron transfer rates (ETR) at different light intensities in barley. Light-adapted barley plants were exposed to increasing light intensities (red actinic light with a wavelength of 620 nm), starting at growth light. A, the qE component of NPQ. B, electron transfer rates of PSII (ETR(II)). C, electron transfer rates of PSI (ETR(I)). Values are means ± SEM (n=4-5, each with >4 technical replicates).



1

Figure 7. P700+ reduction kinetics in barley. A, P700+ reduction in growth light conditions. B, P700+ reduction in high light conditions. Plants were light adapted for >2 h prior measurements, then pre-illuminated with red actinic light (620 nm) for 3 min, followed by a 10 ms dark pulse. The plotted transients are averaged (n=5, each with >4 technical replicates).



1

Figure 8. Photosynthetic regulation in response to phosphorus deficiency at growth light conditions. A, photosynthetic electron flow under sufficient P conditions. B, feedback mechanisms responsible for reduced electron flow from PSII to PSI under P deficiency conditions. See text for further explanation of the cascade of events highlighted in step 1-7.



Parsed CitationsAntal TK, Osipov V, Matorin DN, Rubin AB (2011) Membrane potential is involved in regulation of photosynthetic reactions in themarine diatom Thalassiosira weissflogii. J Photochem Photobiol B Biol 102: 169–173

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Baker A, Ceasar SA, Palmer AJ, Paterson JB, Qi W, Muench SP, Baldwin SA (2015) Replace, reuse, recycle: Improving the sustainableuse of phosphorus by plants. J Exp Bot 66: 3523–3540


Belatik A, Joly D, Hotchandani S, Carpentier R (2013) Re-evaluation of the side effects of cytochrome b6f inhibitordibromothymoquinone on photosystem II excitation and electron transfer. Photosynth Res 117: 489–496


Briantais JM, Vernotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolatedchloroplasts. BBA - Bioenerg 548: 128–138


Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305


Cordell D, White S (2015) Tracking phosphorus security: indicators of phosphorus vulnerability in the global food system. Food Secur7: 337–350


Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis forenergy production and photoprotection. J Exp Bot 56: 395–406


Cruz JA, Sacksteder CA, Kanazawa A, Kramer DM (2001) Contribution of electric field (∆ψ) to steady-state transthylakoid proton motiveforce (pmf) in vitro and in vivo. Control of pmf parsing into ∆ψ and ∆pH by ionic strength. Biochemistry 40: 1226–1237


Damkjaer JT, Kereiche S, Johnson MP, Kovacs L, Kiss AZ, Boekema EJ, Ruban A V., Horton P, Jansson S (2009) The photosystem IIlight-harvesting protein lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in arabidopsis. Plant Cell21: 3245–3256


Duysens LNM, Sweers HE (1963) Mechanism of two photochemical reactions in algae as studied by means of fluorescence. Studmicroalgae Photosynth Bact 353–372


Franck F, Juneau P, Popovic R (2002) Resolution of the Photosystem I and Photosystem II contributions to chlorophyll fluorescence ofintact leaves at room temperature. Biochim Biophys Acta - Bioenerg 1556: 239–246


Frydenvang J, van Maarschalkerweerd M, Carstensen A, Mundus S, Schmidt SB, Pedas PR, Laursen KH, Schjoerring JK, Husted S(2015) Sensitive Detection of Phosphorus Deficiency in Plants Using Chlorophyll a Fluorescence. Plant Physiol 169: 353–61



http://www.ncbi.nlm.nih.gov/pubmed?term=Antal TK%2C Osipov V%2C Matorin DN%2C Rubin AB %282011%29 Membrane potential is involved in regulation of photosynthetic reactions in the marine diatom Thalassiosira weissflogii%2E J Photochem Photobiol B Biol 102%3A 169�??173&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Antal TK, Osipov V, Matorin DN, Rubin AB (2011) Membrane potential is involved in regulation of photosynthetic reactions in the marine diatom Thalassiosira weissflogii. J Photochem Photobiol B Biol 102: 169?173

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Antal&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Membrane potential is involved in regulation of photosynthetic reactions in the marine diatom Thalassiosira weissflogii.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Membrane potential is involved in regulation of photosynthetic reactions in the marine diatom Thalassiosira weissflogii.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Antal&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Baker A%2C Ceasar SA%2C Palmer AJ%2C Paterson JB%2C Qi W%2C Muench SP%2C Baldwin SA %282015%29 Replace%2C reuse%2C recycle%3A Improving the sustainable use of phosphorus by plants%2E J Exp Bot 66%3A 3523�??3540&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Baker A, Ceasar SA, Palmer AJ, Paterson JB, Qi W, Muench SP, Baldwin SA (2015) Replace, reuse, recycle: Improving the sustainable use of phosphorus by plants. J Exp Bot 66: 3523?3540

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Baker&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Replace, reuse, recycle: Improving the sustainable use of phosphorus by plants.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Replace, reuse, recycle: Improving the sustainable use of phosphorus by plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Baker&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Belatik A%2C Joly D%2C Hotchandani S%2C Carpentier R %282013%29 Re%2Devaluation of the side effects of cytochrome b6f inhibitor dibromothymoquinone on photosystem II excitation and electron transfer%2E Photosynth Res 117%3A 489�??496&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Belatik A, Joly D, Hotchandani S, Carpentier R (2013) Re-evaluation of the side effects of cytochrome b6f inhibitor dibromothymoquinone on photosystem II excitation and electron transfer. Photosynth Res 117: 489?496

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Belatik&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Re-evaluation of the side effects of cytochrome b6f inhibitor dibromothymoquinone on photosystem II excitation and electron transfer.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Re-evaluation of the side effects of cytochrome b6f inhibitor dibromothymoquinone on photosystem II excitation and electron transfer.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Belatik&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Briantais JM%2C Vernotte C%2C Picaud M%2C Krause GH %281979%29 A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts%2E BBA %2D Bioenerg 548%3A 128�??138&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Briantais JM, Vernotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. BBA - Bioenerg 548: 128?138

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Briantais&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Briantais&as_ylo=1979&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Cordell D%2C Drangert JO%2C White S %282009%29 The story of phosphorus%3A global food security and food for thought%2E Glob Environ Chang 19%3A 292�??305&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19: 292?305

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Cordell&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The story of phosphorus: global food security and food for thought.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The story of phosphorus: global food security and food for thought.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cordell&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Cordell D%2C White S %282015%29 Tracking phosphorus security%3A indicators of phosphorus vulnerability in the global food system%2E Food Secur 7%3A 337�??350&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cordell D, White S (2015) Tracking phosphorus security: indicators of phosphorus vulnerability in the global food system. Food Secur 7: 337?350

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Cordell&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Tracking phosphorus security: indicators of phosphorus vulnerability in the global food system.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Tracking phosphorus security: indicators of phosphorus vulnerability in the global food system.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cordell&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Cruz JA%2C Avenson TJ%2C Kanazawa A%2C Takizawa K%2C Edwards GE%2C Kramer DM %282005%29 Plasticity in light reactions of photosynthesis for energy production and photoprotection%2E J Exp Bot 56%3A 395�??406&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis for energy production and photoprotection. J Exp Bot 56: 395?406

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Cruz&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Plasticity in light reactions of photosynthesis for energy production and photoprotection.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Plasticity in light reactions of photosynthesis for energy production and photoprotection.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cruz&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Cruz JA%2C Sacksteder CA%2C Kanazawa A%2C Kramer DM %282001%29 Contribution of electric field %28�??�?%29 to steady%2Dstate transthylakoid proton motive force %28pmf%29 in vitro and in vivo%2E Control of pmf parsing into �??�? and �??pH by ionic strength%2E Biochemistry 40%3A 1226�??1237&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cruz JA, Sacksteder CA, Kanazawa A, Kramer DM (2001) Contribution of electric field (??) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into ?? and ?pH by ionic strength. Biochemistry 40: 1226?1237

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Cruz&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Contribution of electric field (â�?�?Ï�?) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Contribution of electric field (â�?�?Ï�?) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cruz&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Damkjaer JT%2C Kereiche S%2C Johnson MP%2C Kovacs L%2C Kiss AZ%2C Boekema EJ%2C Ruban A V%2E%2C Horton P%2C Jansson S %282009%29 The photosystem II light%2Dharvesting protein lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in arabidopsis%2E Plant Cell 21%3A 3245�??3256&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Damkjaer JT, Kereiche S, Johnson MP, Kovacs L, Kiss AZ, Boekema EJ, Ruban A V., Horton P, Jansson S (2009) The photosystem II light-harvesting protein lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in arabidopsis. Plant Cell 21: 3245?3256

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Damkjaer&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The photosystem II light-harvesting protein lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The photosystem II light-harvesting protein lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Damkjaer&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Duysens LNM%2C Sweers HE %281963%29 Mechanism of two photochemical reactions in algae as studied by means of fluorescence%2E Stud microalgae Photosynth Bact 353�??372&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Duysens LNM, Sweers HE (1963) Mechanism of two photochemical reactions in algae as studied by means of fluorescence. Stud microalgae Photosynth Bact 353?372

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Duysens&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mechanism of two photochemical reactions in algae as studied by means of fluorescence.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mechanism of two photochemical reactions in algae as studied by means of fluorescence.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Duysens&as_ylo=1963&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Franck F%2C Juneau P%2C Popovic R %282002%29 Resolution of the Photosystem I and Photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature%2E Biochim Biophys Acta %2D Bioenerg 1556%3A 239�??246&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Franck F, Juneau P, Popovic R (2002) Resolution of the Photosystem I and Photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochim Biophys Acta - Bioenerg 1556: 239?246

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Franck&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Resolution of the Photosystem I and Photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Resolution of the Photosystem I and Photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Franck&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Frydenvang J%2C van Maarschalkerweerd M%2C Carstensen A%2C Mundus S%2C Schmidt SB%2C Pedas PR%2C Laursen KH%2C Schjoerring JK%2C Husted S %282015%29 Sensitive Detection of Phosphorus Deficiency in Plants Using Chlorophyll a Fluorescence%2E Plant Physiol 169%3A 353�??61&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Frydenvang J, van Maarschalkerweerd M, Carstensen A, Mundus S, Schmidt SB, Pedas PR, Laursen KH, Schjoerring JK, Husted S (2015) Sensitive Detection of Phosphorus Deficiency in Plants Using Chlorophyll a Fluorescence. Plant Physiol 169: 353?61

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Frydenvang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Sensitive Detection of Phosphorus Deficiency in Plants Using Chlorophyll a Fluorescence.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Sensitive Detection of Phosphorus Deficiency in Plants Using Chlorophyll a Fluorescence.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Frydenvang&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1


Gilbert N (2009) The disappearing nutrient. Nature 461: 716–718Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescenceand its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol 63: 869–893


Grennan AK, Ort DR (2011) Measurement of chloroplast ATP synthesis activity in arabidopsis. In PR Jarvis, ed, Chloroplast Res. Arab. -Metod. Protoc. vol II. Humana Press, pp 343–355


Guo B, Jin Y, Wussler C, Blancaflor E, Motes C, Versaw W (2008) Functional analysis of the Arabidopsis PHT4 family of intracellularphosphate transporters. New Phytol 177: 889–898


Hammond JP, White PJ (2008) Sucrose transport in the phloem: Integrating root responses to phosphorus starvation. J Exp Bot 59: 93–109


Hawkesford M, Parmar S, Buchner P (2013) Mineral composition analysis: Measuring anion uptake and anion concentrations in planttissues. In JM Walker, ed, Plant Miner. Nutr. Humana Press, York, UK, pp 109–119


Heldt HW, Chon CJ, Maronde D, Herold A, Stankovic ZS, Walker DA, Kraminer A, Kirk MR, Heber U (1977) Role of orthophosphate andother factors in the regulation of starch formation in leaves and isolated chloroplasts. Plant Physiol 59: 1146–1155


Ihnatowicz A, Pesaresi P, Leister D (2007) The E subunit of photosystem I is not essential for linear electron flow and photoautotrophicgrowth in Arabidopsis thaliana. Planta 226: 889–895


Ihnatowicz A, Pesaresi P, Varotto C, Richly E, Schneider A, Jahns P, Salamini F, Leister D (2004) Mutants for photosystem I subunit D ofArabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions.plant J 37: 839–852


Karlsson PM, Herdean A, Adolfsson L, Beebo A, Nziengui H, Irigoyen S, Ünnep R, Zsiros O, Garab G, Aronsson H, et al (2015) TheArabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth. plant J 84: 99–110


Lauer MJ, Pallardy SG, Blevins DG, Randall DD (1989) Whole leaf carbon exchange characteristics of phosphate deficient soybeans(Glycine max L.). Plant Physiol 91: 848–854


Lavorel J, Etienne AL (1977) In vivo chlorophyll fluorescence. Prim Process Photosynth 2: 203–268Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller H V, Scheller H V. (2000) The PSI-H subunit of photosystem I is essential for statetransitions in plant photosynthesis. Nature 408: 613–5

Pubmed: Author and TitleCrossRef: Author and Title www.plantphysiol.orgon September 3, 2020 - Published by Downloaded from

Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Gilbert N %282009%29 The disappearing nutrient%2E Nature 461%3A 716�??718&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Gilbert N (2009) The disappearing nutrient. Nature 461: 716?718

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Gilbert&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The disappearing nutrient.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The disappearing nutrient.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gilbert&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Goltsev VN%2C Kalaji HM%2C Paunov M%2C B�?ba W%2C Horaczek T%2C Mojski J%2C Kociel H%2C Allakhverdiev SI %282016%29 Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus%2E Russ J Plant Physiol 63%3A 869�??893&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Goltsev VN, Kalaji HM, Paunov M, B?ba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol 63: 869?893

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Goltsev&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Goltsev&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Grennan AK%2C Ort DR %282011%29 Measurement of chloroplast ATP synthesis activity in arabidopsis%2E In PR Jarvis%2C ed%2C Chloroplast Res%2E Arab%2E %2D Metod%2E Protoc%2E vol II%2E Humana Press%2C pp 343�??355&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Grennan AK, Ort DR (2011) Measurement of chloroplast ATP synthesis activity in arabidopsis. In PR Jarvis, ed, Chloroplast Res. Arab. - Metod. Protoc. vol II. Humana Press, pp 343?355

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Grennan&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Measurement of chloroplast ATP synthesis activity in arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Measurement of chloroplast ATP synthesis activity in arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Grennan&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Guo B%2C Jin Y%2C Wussler C%2C Blancaflor E%2C Motes C%2C Versaw W %282008%29 Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters%2E New Phytol 177%3A 889�??898&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Guo B, Jin Y, Wussler C, Blancaflor E, Motes C, Versaw W (2008) Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol 177: 889?898

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Guo&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Guo&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Hammond JP%2C White PJ %282008%29 Sucrose transport in the phloem%3A Integrating root responses to phosphorus starvation%2E J Exp Bot 59%3A 93�??109&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hammond JP, White PJ (2008) Sucrose transport in the phloem: Integrating root responses to phosphorus starvation. J Exp Bot 59: 93?109

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hammond&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Sucrose transport in the phloem: Integrating root responses to phosphorus starvation.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Sucrose transport in the phloem: Integrating root responses to phosphorus starvation.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hammond&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Hawkesford M%2C Parmar S%2C Buchner P %282013%29 Mineral composition analysis%3A Measuring anion uptake and anion concentrations in plant tissues%2E In JM Walker%2C ed%2C Plant Miner%2E Nutr%2E Humana Press%2C York%2C UK%2C pp 109�??119&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hawkesford M, Parmar S, Buchner P (2013) Mineral composition analysis: Measuring anion uptake and anion concentrations in plant tissues. In JM Walker, ed, Plant Miner. Nutr. Humana Press, York, UK, pp 109?119

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hawkesford&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mineral composition analysis: Measuring anion uptake and anion concentrations in plant tissues.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mineral composition analysis: Measuring anion uptake and anion concentrations in plant tissues.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hawkesford&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Heldt HW%2C Chon CJ%2C Maronde D%2C Herold A%2C Stankovic ZS%2C Walker DA%2C Kraminer A%2C Kirk MR%2C Heber U %281977%29 Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts%2E Plant Physiol 59%3A 1146�??1155&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Heldt HW, Chon CJ, Maronde D, Herold A, Stankovic ZS, Walker DA, Kraminer A, Kirk MR, Heber U (1977) Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts. Plant Physiol 59: 1146?1155

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Heldt&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Heldt&as_ylo=1977&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ihnatowicz A%2C Pesaresi P%2C Leister D %282007%29 The E subunit of photosystem I is not essential for linear electron flow and photoautotrophic growth in Arabidopsis thaliana%2E Planta 226%3A 889�??895&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ihnatowicz A, Pesaresi P, Leister D (2007) The E subunit of photosystem I is not essential for linear electron flow and photoautotrophic growth in Arabidopsis thaliana. Planta 226: 889?895

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ihnatowicz&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The E subunit of photosystem I is not essential for linear electron flow and photoautotrophic growth in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The E subunit of photosystem I is not essential for linear electron flow and photoautotrophic growth in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ihnatowicz&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ihnatowicz A%2C Pesaresi P%2C Varotto C%2C Richly E%2C Schneider A%2C Jahns P%2C Salamini F%2C Leister D %282004%29 Mutants for photosystem I subunit D of Arabidopsis thaliana%3A effects on photosynthesis%2C photosystem I stability and expression of nuclear genes for chloroplast functions%2E plant J 37%3A 839�??852&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ihnatowicz A, Pesaresi P, Varotto C, Richly E, Schneider A, Jahns P, Salamini F, Leister D (2004) Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions. plant J 37: 839?852

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ihnatowicz&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ihnatowicz&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Karlsson PM%2C Herdean A%2C Adolfsson L%2C Beebo A%2C Nziengui H%2C Irigoyen S%2C �?nnep R%2C Zsiros O%2C Garab G%2C Aronsson H%2C et al %282015%29 The Arabidopsis thylakoid transporter PHT4%3B1 influences phosphate availability for ATP synthesis and plant growth%2E plant J 84%3A 99�??110&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Karlsson PM, Herdean A, Adolfsson L, Beebo A, Nziengui H, Irigoyen S, �nnep R, Zsiros O, Garab G, Aronsson H, et al (2015) The Arabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth. plant J 84: 99?110

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Karlsson&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The Arabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Arabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Karlsson&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lauer MJ%2C Pallardy SG%2C Blevins DG%2C Randall DD %281989%29 Whole leaf carbon exchange characteristics of phosphate deficient soybeans %28Glycine max L%2E%29%2E Plant Physiol 91%3A 848�??854&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lauer MJ, Pallardy SG, Blevins DG, Randall DD (1989) Whole leaf carbon exchange characteristics of phosphate deficient soybeans (Glycine max L.). Plant Physiol 91: 848?854

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lauer&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Whole leaf carbon exchange characteristics of phosphate deficient soybeans (Glycine max L.).&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Whole leaf carbon exchange characteristics of phosphate deficient soybeans (Glycine max L.).&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lauer&as_ylo=1989&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lavorel J%2C Etienne AL %281977%29 In vivo chlorophyll fluorescence%2E Prim Process Photosynth 2%3A 203�??268&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lavorel J, Etienne AL (1977) In vivo chlorophyll fluorescence. Prim Process Photosynth 2: 203?268

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lavorel&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=In vivo chlorophyll fluorescence.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=In vivo chlorophyll fluorescence.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lavorel&as_ylo=1977&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lunde C%2C Jensen PE%2C Haldrup A%2C Knoetzel J%2C Scheller H V%2C Scheller H V%2E %282000%29 The PSI%2DH subunit of photosystem I is essential for state transitions in plant photosynthesis%2E Nature 408%3A 613�??5&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller H V, Scheller H V. (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408: 613?5


Google Scholar: Author Only Title Only Author and Title

MacDonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances across the world’s croplands. ProcNatl Acad Sci U S A 108: 3086–91


Mimura T, Dietz K-J, Kaiser W, Schramm MJ, Kaiser G, Heber U (1990) Phosphate transport across biomembranes and cytosolicphosphate homeostasis in barley leaves. Planta 180: 139–146


Młodzińska E, Zboińska M (2016) Phosphate Uptake and Allocation - A Closer Look at Arabidopsis thaliana L. and Oryza sativa L. FrontPlant Sci 7: 1198


Muneer S, Jeong BR (2015) Proteomic analysis provides new insights in phosphorus homeostasis subjected to pi (inorganicphosphate) starvation in tomato plants (Solanum lycopersicum L.). PLoS One 10: 1–18


Müller P, Li X, Niyogi KK (2001) Update on photosynthesis non-photochemical quenching. A response to excess light energy. PlantPhysiol 125: 1558–1566


Pavón LR, Lundh F, Lundin B, Mishra A, Persson BL, Spetea C (2008) Arabidopsis ANTR1 is a thylakoid Na+-dependent phosphatetransporter: Functional characterization in Escherichia coli. J Biol Chem 283: 13520–13527


Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations forassaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards byatomic absorption spectroscopy. Biochim Biophys Acta 975: 384–394


Queval G, Noctor G (2007) A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts:application to redox profiling during Arabidopsis rosette development. Anal Biochem 363: 58–69


Ramaekers L, Remans R, Rao IM, Blair MW, Vanderleyden J (2010) Strategies for improving phosphorus acquisition efficiency of cropplants. F Crop Res 117: 169–176


Rao IM, Terry N (1995) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet (IV. changes with time followingincreased supply of phosphate to low-phosphate plants). Plant Physiol 107: 1313–1321


Reich PB, Oleksyn J, Wright IJ (2009) Leaf phosphorus influences the photosynthesis-nitrogen relation: A cross-biome analysis of 314species. Oecologia 160: 207–212


Reuter DJ, Robinson JB (1997) Plant analysis: An interpretation manual, 2nd ed. CSIRO publishing, Collingwood, AustraliaPubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Robinson C, Mant A (2002) Molecular plant biology - A practical approach. Oxford Universiy Press www.plantphysiol.orgon September 3, 2020 - Published by Downloaded from

Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lunde&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lunde&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=MacDonald GK%2C Bennett EM%2C Potter PA%2C Ramankutty N %282011%29 Agronomic phosphorus imbalances across the world�??s croplands%2E Proc Natl Acad Sci U S A 108%3A 3086�??91&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=MacDonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances across the world?s croplands. Proc Natl Acad Sci U S A 108: 3086?91

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=MacDonald&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Agronomic phosphorus imbalances across the worldâ�?�?s croplands.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Agronomic phosphorus imbalances across the worldâ�?�?s croplands.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=MacDonald&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Mimura T%2C Dietz K%2DJ%2C Kaiser W%2C Schramm MJ%2C Kaiser G%2C Heber U %281990%29 Phosphate transport across biomembranes and cytosolic phosphate homeostasis in barley leaves%2E Planta 180%3A 139�??146&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mimura T, Dietz K-J, Kaiser W, Schramm MJ, Kaiser G, Heber U (1990) Phosphate transport across biomembranes and cytosolic phosphate homeostasis in barley leaves. Planta 180: 139?146

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Mimura&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Phosphate transport across biomembranes and cytosolic phosphate homeostasis in barley leaves.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Phosphate transport across biomembranes and cytosolic phosphate homeostasis in barley leaves.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mimura&as_ylo=1990&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=M�?odzi�?ska E%2C Zboi�?ska M %282016%29 Phosphate Uptake and Allocation %2D A Closer Look at Arabidopsis thaliana L%2E and Oryza sativa L%2E Front Plant Sci 7%3A 1198&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=M?odzi?ska E, Zboi?ska M (2016) Phosphate Uptake and Allocation - A Closer Look at Arabidopsis thaliana L. and Oryza sativa L. Front Plant Sci 7: 1198

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=M�?�?odzi�?�?ska&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Phosphate Uptake and Allocation - A Closer Look at Arabidopsis thaliana L.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Phosphate Uptake and Allocation - A Closer Look at Arabidopsis thaliana L.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=M�?�?odzi�?�?ska&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Muneer S%2C Jeong BR %282015%29 Proteomic analysis provides new insights in phosphorus homeostasis subjected to pi %28inorganic phosphate%29 starvation in tomato plants %28Solanum lycopersicum L%2E%29%2E PLoS One 10%3A 1�??18&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Muneer S, Jeong BR (2015) Proteomic analysis provides new insights in phosphorus homeostasis subjected to pi (inorganic phosphate) starvation in tomato plants (Solanum lycopersicum L.). PLoS One 10: 1?18

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Muneer&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Proteomic analysis provides new insights in phosphorus homeostasis subjected to pi (inorganic phosphate) starvation in tomato plants (Solanum lycopersicum L.).&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Proteomic analysis provides new insights in phosphorus homeostasis subjected to pi (inorganic phosphate) starvation in tomato plants (Solanum lycopersicum L.).&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Muneer&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Müller P%2C Li X%2C Niyogi KK %282001%29 Update on photosynthesis non%2Dphotochemical quenching%2E A response to excess light energy%2E Plant Physiol 125%3A 1558�??1566&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=M�ller P, Li X, Niyogi KK (2001) Update on photosynthesis non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558?1566

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=M�?¼ller&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Update on photosynthesis non-photochemical quenching.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Update on photosynthesis non-photochemical quenching.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=M�?¼ller&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pavón LR%2C Lundh F%2C Lundin B%2C Mishra A%2C Persson BL%2C Spetea C %282008%29 Arabidopsis ANTR1 is a thylakoid Na%2B%2Ddependent phosphate transporter%3A Functional characterization in Escherichia coli%2E J Biol Chem 283%3A 13520�??13527&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pav�n LR, Lundh F, Lundin B, Mishra A, Persson BL, Spetea C (2008) Arabidopsis ANTR1 is a thylakoid Na+-dependent phosphate transporter: Functional characterization in Escherichia coli. J Biol Chem 283: 13520?13527

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Pav�?³n&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis ANTR1 is a thylakoid Na+-dependent phosphate transporter: Functional characterization in Escherichia coli.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis ANTR1 is a thylakoid Na+-dependent phosphate transporter: Functional characterization in Escherichia coli.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pav�?³n&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Porra RJ%2C Thompson WA%2C Kriedemann PE %281989%29 Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents%3A verification of the concentration of chlorophyll standards by atomic absorption spectroscopy%2E Biochim Biophys Acta 975%3A 384�??394&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384?394

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Porra&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Porra&as_ylo=1989&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Queval G%2C Noctor G %282007%29 A plate reader method for the measurement of NAD%2C NADP%2C glutathione%2C and ascorbate in tissue extracts%3A application to redox profiling during Arabidopsis rosette development%2E Anal Biochem 363%3A 58�??69&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Queval G, Noctor G (2007) A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. Anal Biochem 363: 58?69

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Queval&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Queval&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ramaekers L%2C Remans R%2C Rao IM%2C Blair MW%2C Vanderleyden J %282010%29 Strategies for improving phosphorus acquisition efficiency of crop plants%2E F Crop Res 117%3A 169�??176&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ramaekers L, Remans R, Rao IM, Blair MW, Vanderleyden J (2010) Strategies for improving phosphorus acquisition efficiency of crop plants. F Crop Res 117: 169?176

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ramaekers&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Strategies for improving phosphorus acquisition efficiency of crop plants.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Strategies for improving phosphorus acquisition efficiency of crop plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ramaekers&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Rao IM%2C Terry N %281995%29 Leaf phosphate status%2C photosynthesis%2C and carbon partitioning in sugar beet %28IV%2E changes with time following increased supply of phosphate to low%2Dphosphate plants%29%2E Plant Physiol 107%3A 1313�??1321&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rao IM, Terry N (1995) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet (IV. changes with time following increased supply of phosphate to low-phosphate plants). Plant Physiol 107: 1313?1321

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Rao&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet (IV.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet (IV.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rao&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Reich PB%2C Oleksyn J%2C Wright IJ %282009%29 Leaf phosphorus influences the photosynthesis%2Dnitrogen relation%3A A cross%2Dbiome analysis of 314 species%2E Oecologia 160%3A 207�??212&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Reich PB, Oleksyn J, Wright IJ (2009) Leaf phosphorus influences the photosynthesis-nitrogen relation: A cross-biome analysis of 314 species. Oecologia 160: 207?212

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Reich&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Leaf phosphorus influences the photosynthesis-nitrogen relation: A cross-biome analysis of 314 species.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Leaf phosphorus influences the photosynthesis-nitrogen relation: A cross-biome analysis of 314 species.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Reich&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Reuter DJ%2C Robinson JB %281997%29 Plant analysis%3A An interpretation manual%2C 2nd ed%2E CSIRO publishing%2C Collingwood%2C Australia&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Reuter DJ, Robinson JB (1997) Plant analysis: An interpretation manual, 2nd ed. CSIRO publishing, Collingwood, Australia

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Reuter&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Plant analysis: An interpretation manual, 2nd ed.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Plant analysis: An interpretation manual, 2nd ed.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Reuter&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1



Robinson SP, Giersch C (1987) Inorganic phosphate concentration in the stroma of isolated chloroplasts and its influence onphotosynthesis. Aust J Pant Physiol 14: 451–62


Ruban A V (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants fromphotodamage. Plant Physiol 170: 1903–1916


Rychter AM, Rao IM (2005) Role of phosphorus in photosynthetic carbon metabolism. In M Pessarakli, ed, Handb. Photosynth., 2nd ed.CRC Press, pp 123–148


Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role ofphotosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta - Bioenerg 1706: 250–261


Schlodder E, Meyer B (1987) pH dependence of oxygen evolution and reduction kinetics of photooxidized chlorophyll aII (P-680) inphotosystem II particles from Synechococcus sp. Biochim Biophys Acta 890: 23–31


Sharkey TD, Vanderveer PJ (1989) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiol 91:679–684


Smith AM, Zeeman SC (2006) Quantification of starch in plant tissues. Nat Protoc 1: 1342–1345Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Srivastava A, Strasser RJ, Govindjee (1995) Polyphasic rise of chlorophyll a fluorescence in herbicide-resistant D1 mutants ofChlamydomonas reinardtii. Photosynth Res 43: 131–141


Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise.Photosynth Res 113: 15–61


Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II:Basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B Biol 104: 236–257


Stirbet A, Riznichenko G, Rubin A, Govindjee (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis.Biochemistry 79: 291–323


Strand DD, Fisher N, Kramer DM (2017) The higher plant plastid NAD(P)H dehydrogenase-like complex (NDH) is a high efficiencyproton pump that increases ATP production by cyclic electron flow. J Biol Chem 292: 11850–11860


Strand DD, Kramer DM (2014) Control of non-photochemical exciton quenching by the proton circuit of photosynthesis. In B Demmig- www.plantphysiol.orgon September 3, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Robinson C%2C Mant A %282002%29 Molecular plant biology %2D A practical approach%2E Oxford Universiy Press&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Robinson C, Mant A (2002) Molecular plant biology - A practical approach. Oxford Universiy Press

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Robinson&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Molecular plant biology - A practical approach.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Molecular plant biology - A practical approach.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Robinson&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Robinson SP%2C Giersch C %281987%29 Inorganic phosphate concentration in the stroma of isolated chloroplasts and its influence on photosynthesis%2E Aust J Pant Physiol 14%3A 451�??62&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Robinson SP, Giersch C (1987) Inorganic phosphate concentration in the stroma of isolated chloroplasts and its influence on photosynthesis. Aust J Pant Physiol 14: 451?62

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Robinson&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Inorganic phosphate concentration in the stroma of isolated chloroplasts and its influence on photosynthesis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Inorganic phosphate concentration in the stroma of isolated chloroplasts and its influence on photosynthesis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Robinson&as_ylo=1987&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ruban A V %282016%29 Nonphotochemical chlorophyll fluorescence quenching%3A mechanism and effectiveness in protecting plants from photodamage%2E Plant Physiol 170%3A 1903�??1916&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ruban A V (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170: 1903?1916

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ruban&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ruban&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Rychter AM%2C Rao IM %282005%29 Role of phosphorus in photosynthetic carbon metabolism%2E In M Pessarakli%2C ed%2C Handb%2E Photosynth%2E%2C 2nd ed%2E CRC Press%2C pp 123�??148&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rychter AM, Rao IM (2005) Role of phosphorus in photosynthetic carbon metabolism. In M Pessarakli, ed, Handb. Photosynth., 2nd ed. CRC Press, pp 123?148

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Rychter&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Role of phosphorus in photosynthetic carbon metabolism.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Role of phosphorus in photosynthetic carbon metabolism.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rychter&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schansker G%2C Tóth SZ%2C Strasser RJ %282005%29 Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP%2E Biochim Biophys Acta %2D Bioenerg 1706%3A 250�??261&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schansker G, T�th SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta - Bioenerg 1706: 250?261

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Schansker&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schansker&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schlodder E%2C Meyer B %281987%29 pH dependence of oxygen evolution and reduction kinetics of photooxidized chlorophyll aII %28P%2D680%29 in photosystem II particles from Synechococcus sp%2E Biochim Biophys Acta 890%3A 23�??31&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schlodder E, Meyer B (1987) pH dependence of oxygen evolution and reduction kinetics of photooxidized chlorophyll aII (P-680) in photosystem II particles from Synechococcus sp. Biochim Biophys Acta 890: 23?31

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Schlodder&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=pH dependence of oxygen evolution and reduction kinetics of photooxidized chlorophyll aII (P-680) in photosystem II particles from Synechococcus sp.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=pH dependence of oxygen evolution and reduction kinetics of photooxidized chlorophyll aII (P-680) in photosystem II particles from Synechococcus sp.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schlodder&as_ylo=1987&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sharkey TD%2C Vanderveer PJ %281989%29 Stromal phosphate concentration is low during feedback limited photosynthesis%2E Plant Physiol 91%3A 679�??684&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sharkey TD, Vanderveer PJ (1989) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiol 91: 679?684

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Sharkey&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Stromal phosphate concentration is low during feedback limited photosynthesis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Stromal phosphate concentration is low during feedback limited photosynthesis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sharkey&as_ylo=1989&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Smith AM%2C Zeeman SC %282006%29 Quantification of starch in plant tissues%2E Nat Protoc 1%3A 1342�??1345&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Smith AM, Zeeman SC (2006) Quantification of starch in plant tissues. Nat Protoc 1: 1342?1345

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Smith&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Quantification of starch in plant tissues.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Quantification of starch in plant tissues.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Smith&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Srivastava A%2C Strasser RJ%2C Govindjee %281995%29 Polyphasic rise of chlorophyll a fluorescence in herbicide%2Dresistant D1 mutants of Chlamydomonas reinardtii%2E Photosynth Res 43%3A 131�??141&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Srivastava A, Strasser RJ, Govindjee (1995) Polyphasic rise of chlorophyll a fluorescence in herbicide-resistant D1 mutants of Chlamydomonas reinardtii. Photosynth Res 43: 131?141

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Srivastava&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Polyphasic rise of chlorophyll a fluorescence in herbicide-resistant D1 mutants of Chlamydomonas reinardtii.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Polyphasic rise of chlorophyll a fluorescence in herbicide-resistant D1 mutants of Chlamydomonas reinardtii.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Srivastava&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Stirbet A%2C Govindjee %282012%29 Chlorophyll a fluorescence induction%3A a personal perspective of the thermal phase%2C the J%2DI%2DP rise%2E Photosynth Res 113%3A 15�??61&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res 113: 15?61

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Stirbet&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Stirbet&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Stirbet A%2C Govindjee %282011%29 On the relation between the Kautsky effect %28chlorophyll a fluorescence induction%29 and Photosystem II%3A Basics and applications of the OJIP fluorescence transient%2E J Photochem Photobiol B Biol 104%3A 236�??257&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B Biol 104: 236?257


http://scholar.google.com/scholar?as_q=On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Stirbet&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Stirbet A%2C Riznichenko G%2C Rubin A%2C Govindjee %282014%29 Modeling chlorophyll a fluorescence transient%3A relation to photosynthesis%2E Biochemistry 79%3A 291�??323&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Stirbet A, Riznichenko G, Rubin A, Govindjee (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochemistry 79: 291?323


http://scholar.google.com/scholar?as_q=Modeling chlorophyll a fluorescence transient: relation to photosynthesis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Modeling chlorophyll a fluorescence transient: relation to photosynthesis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Stirbet&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Strand DD%2C Fisher N%2C Kramer DM %282017%29 The higher plant plastid NAD%28P%29H dehydrogenase%2Dlike complex %28NDH%29 is a high efficiency proton pump that increases ATP production by cyclic electron flow%2E J Biol Chem 292%3A 11850�??11860&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Strand DD, Fisher N, Kramer DM (2017) The higher plant plastid NAD(P)H dehydrogenase-like complex (NDH) is a high efficiency proton pump that increases ATP production by cyclic electron flow. J Biol Chem 292: 11850?11860

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Strand&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The higher plant plastid NAD(P)H dehydrogenase-like complex (NDH) is a high efficiency proton pump that increases ATP production by cyclic electron flow.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The higher plant plastid NAD(P)H dehydrogenase-like complex (NDH) is a high efficiency proton pump that increases ATP production by cyclic electron flow.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Strand&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1


Adams, G Garab, W Adams, Govindjee, eds, Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria.Springer, pp 387–408


Strasser RJ, Govindjee (1992) The Fo and the O-J-I-P Fluorescence Rise in Higher Plants and Algae. In JH Argyroudi-Akoyunoglou, ed,Regul. Chloroplast Biog. Springer US, Boston, MA, pp 423–426


Takizawa K, Kanazawa A, Kramer DM (2008) Depletion of stromal Pi induces high “energy-dependent” antenna exciton quenching (qE)by decreasing proton conductivity at CFo-CF1 ATP synthase. Plant Cell Environ 31: 235–243


Tietz S, Hall CC, Cruz JA, Kramer DM (2017) NPQ(T): a chlorophyll fluorescence parameter for rapid estimation and imaging of non-photochemical quenching of excitons in photosystem-II-associated antenna complexes. Plant Cell Environ 40: 1243–1255


Tikhonov AN (2013) pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts. Photophysiology 116: 511–534Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Tikhonov AN (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways. Plant PhysiolBiochem 81: 163–183


Tóth SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient.Photosynth Res 93: 193–203


Vredenberg WJ (2004) System analysis and photoelectrochemical control of chlorophyll fluorescence in terms of trapping models ofphotosystem II: a challenging view. Chlorophyll a Fluoresc. Springer, pp 133–172


Walan P, Davidsson S, Johansson S, Höök M (2014) Phosphate rock production and depletion: regional disaggregated modeling andglobal implications. Resour Conserv Recycl 93: 178–187


Yan N, Zhang YL, Xue HM, Zhang XH, Wang ZD, Shi LY, Guo DP (2015) Changes in plant growth and photosynthetic performance ofZizania latifolia exposed to different phosphorus concentrations under hydroponic condition. Photosynthetica 53: 630–635


Yin L, Vener A V, Spetea C (2015) The membrane proteome of stroma thylakoids from Arabidopsis thaliana studied by successive in-solution and in-gel digestion. Physiol Plant 154: 433–446


Zhang K, Liu H, Tao P, Chen H (2014) Comparative proteomic analyses provide new insights into low phosphorus stress responses inmaize leaves. PLoS One 9: 1–16



http://www.ncbi.nlm.nih.gov/pubmed?term=Strand DD%2C Kramer DM %282014%29 Control of non%2Dphotochemical exciton quenching by the proton circuit of photosynthesis%2E In B Demmig%2DAdams%2C G Garab%2C W Adams%2C Govindjee%2C eds%2C Non%2Dphotochemical quenching and energy dissipation in plants%2C algae and cyanobacteria%2E Springer%2C pp 387�??408&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Strand DD, Kramer DM (2014) Control of non-photochemical exciton quenching by the proton circuit of photosynthesis. In B Demmig-Adams, G Garab, W Adams, Govindjee, eds, Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, pp 387?408

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Strand&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Control of non-photochemical exciton quenching by the proton circuit of photosynthesis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Control of non-photochemical exciton quenching by the proton circuit of photosynthesis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Strand&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Strasser RJ%2C Govindjee %281992%29 The Fo and the O%2DJ%2DI%2DP Fluorescence Rise in Higher Plants and Algae%2E In JH Argyroudi%2DAkoyunoglou%2C ed%2C Regul%2E Chloroplast Biog%2E Springer US%2C Boston%2C MA%2C pp 423�??426&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Strasser RJ, Govindjee (1992) The Fo and the O-J-I-P Fluorescence Rise in Higher Plants and Algae. In JH Argyroudi-Akoyunoglou, ed, Regul. Chloroplast Biog. Springer US, Boston, MA, pp 423?426

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Strasser&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The Fo and the O-J-I-P Fluorescence Rise in Higher Plants and Algae.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Fo and the O-J-I-P Fluorescence Rise in Higher Plants and Algae.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Strasser&as_ylo=1992&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Takizawa K%2C Kanazawa A%2C Kramer DM %282008%29 Depletion of stromal Pi induces high �??energy%2Ddependent�?� antenna exciton quenching %28qE%29 by decreasing proton conductivity at CFo%2DCF1 ATP synthase%2E Plant Cell Environ 31%3A 235�??243&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Takizawa K, Kanazawa A, Kramer DM (2008) Depletion of stromal Pi induces high ?energy-dependent? antenna exciton quenching (qE) by decreasing proton conductivity at CFo-CF1 ATP synthase. Plant Cell Environ 31: 235?243

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Takizawa&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Depletion of stromal Pi induces high â�?�?energy-dependentâ�?� antenna exciton quenching (qE) by decreasing proton conductivity at CFo-CF1 ATP synthase.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Depletion of stromal Pi induces high â�?�?energy-dependentâ�?� antenna exciton quenching (qE) by decreasing proton conductivity at CFo-CF1 ATP synthase.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Takizawa&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tietz S%2C Hall CC%2C Cruz JA%2C Kramer DM %282017%29 NPQ%28T%29%3A a chlorophyll fluorescence parameter for rapid estimation and imaging of non%2Dphotochemical quenching of excitons in photosystem%2DII%2Dassociated antenna complexes%2E Plant Cell Environ 40%3A 1243�??1255&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tietz S, Hall CC, Cruz JA, Kramer DM (2017) NPQ(T): a chlorophyll fluorescence parameter for rapid estimation and imaging of non-photochemical quenching of excitons in photosystem-II-associated antenna complexes. Plant Cell Environ 40: 1243?1255

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Tietz&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=NPQ(T): a chlorophyll fluorescence parameter for rapid estimation and imaging of non-photochemical quenching of excitons in photosystem-II-associated antenna complexes.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=NPQ(T): a chlorophyll fluorescence parameter for rapid estimation and imaging of non-photochemical quenching of excitons in photosystem-II-associated antenna complexes.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tietz&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tikhonov AN %282013%29 pH%2DDependent regulation of electron transport and ATP synthesis in chloroplasts%2E Photophysiology 116%3A 511�??534&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tikhonov AN (2013) pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts. Photophysiology 116: 511?534

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Tikhonov&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tikhonov&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tikhonov AN %282014%29 The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways%2E Plant Physiol Biochem 81%3A 163�??183&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tikhonov AN (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways. Plant Physiol Biochem 81: 163?183

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Tikhonov&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tikhonov&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tóth SZ%2C Schansker G%2C Strasser RJ %282007%29 A non%2Dinvasive assay of the plastoquinone pool redox state based on the OJIP%2Dtransient%2E Photosynth Res 93%3A 193�??203&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=T�th SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93: 193?203

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=T�?³th&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=T�?³th&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Vredenberg WJ %282004%29 System analysis and photoelectrochemical control of chlorophyll fluorescence in terms of trapping models of photosystem II%3A a challenging view%2E Chlorophyll a Fluoresc%2E Springer%2C pp 133�??172&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Vredenberg WJ (2004) System analysis and photoelectrochemical control of chlorophyll fluorescence in terms of trapping models of photosystem II: a challenging view. Chlorophyll a Fluoresc. Springer, pp 133?172

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Vredenberg&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=System analysis and photoelectrochemical control of chlorophyll fluorescence in terms of trapping models of photosystem II: a challenging view.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=System analysis and photoelectrochemical control of chlorophyll fluorescence in terms of trapping models of photosystem II: a challenging view.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Vredenberg&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Walan P%2C Davidsson S%2C Johansson S%2C Höök M %282014%29 Phosphate rock production and depletion%3A regional disaggregated modeling and global implications%2E Resour Conserv Recycl 93%3A 178�??187&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Walan P, Davidsson S, Johansson S, H��k M (2014) Phosphate rock production and depletion: regional disaggregated modeling and global implications. Resour Conserv Recycl 93: 178?187

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Walan&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Phosphate rock production and depletion: regional disaggregated modeling and global implications.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Phosphate rock production and depletion: regional disaggregated modeling and global implications.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Walan&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yan N%2C Zhang YL%2C Xue HM%2C Zhang XH%2C Wang ZD%2C Shi LY%2C Guo DP %282015%29 Changes in plant growth and photosynthetic performance of Zizania latifolia exposed to different phosphorus concentrations under hydroponic condition%2E Photosynthetica 53%3A 630�??635&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yan N, Zhang YL, Xue HM, Zhang XH, Wang ZD, Shi LY, Guo DP (2015) Changes in plant growth and photosynthetic performance of Zizania latifolia exposed to different phosphorus concentrations under hydroponic condition. Photosynthetica 53: 630?635

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yan&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Changes in plant growth and photosynthetic performance of Zizania latifolia exposed to different phosphorus concentrations under hydroponic condition.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Changes in plant growth and photosynthetic performance of Zizania latifolia exposed to different phosphorus concentrations under hydroponic condition.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yan&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yin L%2C Vener A V%2C Spetea C %282015%29 The membrane proteome of stroma thylakoids from Arabidopsis thaliana studied by successive in%2Dsolution and in%2Dgel digestion%2E Physiol Plant 154%3A 433�??446&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yin L, Vener A V, Spetea C (2015) The membrane proteome of stroma thylakoids from Arabidopsis thaliana studied by successive in-solution and in-gel digestion. Physiol Plant 154: 433?446

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yin&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The membrane proteome of stroma thylakoids from Arabidopsis thaliana studied by successive in-solution and in-gel digestion.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The membrane proteome of stroma thylakoids from Arabidopsis thaliana studied by successive in-solution and in-gel digestion.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yin&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang K%2C Liu H%2C Tao P%2C Chen H %282014%29 Comparative proteomic analyses provide new insights into low phosphorus stress responses in maize leaves%2E PLoS One 9%3A 1�??16&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang K, Liu H, Tao P, Chen H (2014) Comparative proteomic analyses provide new insights into low phosphorus stress responses in maize leaves. PLoS One 9: 1?16

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Comparative proteomic analyses provide new insights into low phosphorus stress responses in maize leaves.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Comparative proteomic analyses provide new insights into low phosphorus stress responses in maize leaves.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1


Documents

Plant Physiology - The impacts of phosphorus deficiency on ...2018/03/14 · Plant growth under phosphorus deficiency 101 Multiple sets of barley plants (Hordeum vulgare L. cv. Quench)