31
1 Short title: The control of photosynthesis by ethylene 1 Corresponding author 2 Prof. Dr. Ir. Bram Van de Poel 3 Department of Biosystems 4 University of Leuven 5 Willem de Croylaan 42 6 3001 Leuven 7 Belgium 8 [email protected] 9 0032/16325527 10 11 Update: Ethylene exerts species-specific and age-dependent control of 12 photosynthesis 13 14 Ceusters Johan 1,2 & Van de Poel Bram 3,* 15 1 KU Leuven, Department of Microbial and Molecular Systems, Bioengineering Technology TC, 16 Campus Geel, Kleinhoefstraat 4, 2440 Geel, Belgium 17 2 UHasselt, Centre for Environmental Sciences, Environmental Biology, Campus Diepenbeek, 18 Agoralaan Building D, 3590, Diepenbeek, Belgium 19 3 KU Leuven, Department of Biosystems, Willem de Croylaan 42, 3001 Leuven, Belgium 20 *corresponding author: [email protected] 21 One sentence summary 22 Ethylene regulates many different aspects of photosynthesis in an age-dependent and species- 23 specific manner. 24 Author contributions 25 J.C. and B.V.d.P. performed the literature search and wrote the article. 26 Funding information 27 J.C. and B.V.d.P. thank the Research Fund and Internal Fund of KU Leuven for financial support 28 (OT/14/082, STGBF/16/005 and 3H140277) 29 30 Abstract 31 The volatile plant hormone ethylene plays a regulatory role in many developmental processes and in 32 biotic and abiotic stress responses. One of the under-explored actions of ethylene is its regulation of 33 photosynthesis and associated components such as stomatal conductance, chlorophyll content, light 34 reactions, carboxylation events, carbohydrate partitioning, and age-related senescence. In this 35 update, we summarize the current knowledge concerning the regulation of photosynthesis, focusing 36 on the model species Arabidopsis thaliana. We describe how ethylene directs photosynthesis in 37 juvenile non-senescing leaves and mature senescing leaves. Furthermore, we extend these insights 38 Plant Physiology Preview. Published on February 2, 2018, as DOI:10.1104/pp.17.01706 Copyright 2018 by the American Society of Plant Biologists www.plantphysiol.org on March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

Short title: The control of photosynthesis by ethylene · 2 39. to other types of photosynthesis (C4 and crassulacean acid metabolism) and highlight the species-40. specific effect

  • Upload
    lyngoc

  • View
    227

  • Download
    0

Embed Size (px)

Citation preview

1

Short title: The control of photosynthesis by ethylene 1

Corresponding author 2

Prof. Dr. Ir. Bram Van de Poel 3

Department of Biosystems 4

University of Leuven 5

Willem de Croylaan 42 6

3001 Leuven 7

Belgium 8

[email protected] 9

0032/16325527 10 11

Update: Ethylene exerts species-specific and age-dependent control of 12

photosynthesis 13

14

Ceusters Johan1,2 & Van de Poel Bram3,* 15

1 KU Leuven, Department of Microbial and Molecular Systems, Bioengineering Technology TC, 16

Campus Geel, Kleinhoefstraat 4, 2440 Geel, Belgium 17 2 UHasselt, Centre for Environmental Sciences, Environmental Biology, Campus Diepenbeek, 18

Agoralaan Building D, 3590, Diepenbeek, Belgium 19 3 KU Leuven, Department of Biosystems, Willem de Croylaan 42, 3001 Leuven, Belgium 20

*corresponding author: [email protected] 21

One sentence summary 22

Ethylene regulates many different aspects of photosynthesis in an age-dependent and species-23

specific manner. 24

Author contributions 25

J.C. and B.V.d.P. performed the literature search and wrote the article. 26

Funding information 27

J.C. and B.V.d.P. thank the Research Fund and Internal Fund of KU Leuven for financial support 28

(OT/14/082, STGBF/16/005 and 3H140277) 29

30

Abstract 31

The volatile plant hormone ethylene plays a regulatory role in many developmental processes and in 32

biotic and abiotic stress responses. One of the under-explored actions of ethylene is its regulation of 33

photosynthesis and associated components such as stomatal conductance, chlorophyll content, light 34

reactions, carboxylation events, carbohydrate partitioning, and age-related senescence. In this 35

update, we summarize the current knowledge concerning the regulation of photosynthesis, focusing 36

on the model species Arabidopsis thaliana. We describe how ethylene directs photosynthesis in 37

juvenile non-senescing leaves and mature senescing leaves. Furthermore, we extend these insights 38

Plant Physiology Preview. Published on February 2, 2018, as DOI:10.1104/pp.17.01706

Copyright 2018 by the American Society of Plant Biologists

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

2

to other types of photosynthesis (C4 and crassulacean acid metabolism) and highlight the species-39

specific effects of the physiological action of ethylene on this complex metabolic pathway. 40

Introduction 41

The volatile plant hormone ethylene (C2H4) is involved in many cellular and developmental 42

processes, such as germination, root and hypocotyl development, climacteric fruit ripening, and 43

senescence (Abeles et al., 1992; Wen et al., 2015; Van de Poel et al., 2015), as well as in the response 44

to biotic and abiotic stress (Bari & Jones, 2009; Kazan et al., 2015). Photosynthesis is one of the least 45

referenced processes regulated by ethylene, which plays a role in all three carbon fixation pathways 46

used by plants: C3, C4, and crassulacean acid metabolism (CAM) (Box 1). Photosynthesis is a complex 47

autotrophic process mediated by the interplay of factors such as light quantity and quality, 48

atmospheric CO2 concentration, stomatal aperture, chlorophyll content, light harvesting complex 49

efficiency, sugar feedback, water availability, nutrient status, and hormonal cues. The role of 50

ethylene in controlling photosynthesis was first described by Kays and Pallas in 1980, who found that 51

the hormone reduces photosynthesis in peanut (Arachis hypogaea). This hormonal control seems to 52

be an ancient response in plants because ethylene downregulates photosynthesis in the charophyte 53

green algae Spirogyra pratensis, suggesting that the regulation of photosynthesis by ethylene is 54

likely conserved and predates the colonization of non-aquatic habits by plants (Ju et al., 2015; Van 55

de Poel et al., 2016). 56

The effect that ethylene exerts on photosynthesis depends on leaf age (Figure 1). Ethylene directly 57

controls photosynthesis in juvenile non-senescing leaves and acts indirectly in mature leaves by 58

promoting leaf senescence. In this review, we describe the effect of ethylene on young non-59

senescing leaves, focusing on the elements that influence plant photosynthesis (chlorophyll content, 60

stomatal conductance, light dissipation, carbon fixation and carbohydrate partitioning). We also 61

briefly highlight the role of ethylene in leaf senescence and refer the reader to a more specialized 62

review on this topic by Kim et al. (2015). 63

64

Ethylene is essential for normal photosynthesis in Arabidopsis thaliana 65

The molecular regulation of photosynthesis by ethylene has been studied using ethylene-related 66

mutants in Arabidopsis and other model plants. Box 2 highlights the steps of the ethylene signaling 67

pathway. Grbic & Bleecker (1998) initially showed that juvenile non-senescing leaves of the 68

Arabidopsis ethylene-insensitive mutant ethylene resistant 1 (etr1-1) possess lower chlorophyll 69

contents, Rubisco activity, and expression of photosynthetically active genes (PAGs) such as CAB 70

(chlorophyll a/b binding protein) and RUBISCO SS (ribulose bisphosphate carboxylase small subunit), 71

suggesting a role for ethylene in controlling photosynthesis in non-senescing leaves. These results 72

were further corroborated by Tholen et al. (2004, 2007, 2008) who showed that ethylene-insensitive 73

mutants of Arabidopsis (etr1-1 and ethylene insensitive 2, ein2) and ethylene-insensitive transgenic 74

tobacco (Nicotiana tabacum) plants carrying the dominant mutant allele of Arabidopsis etr1-1 have a 75

lower whole-plant and leaf photosynthetic capacity, especially under saturating light conditions. 76

These studies suggest that basal ethylene perception is essential for achieving normal 77

photosynthetic capacity in Arabidopsis leaves. In addition, transient ethylene treatment of non-78

senescing leaves reduces chlorophyll content (Zacarias & Reid, 1990) and downregulates CAB 79

expression in Arabidopsis (Grbic & Bleecker, 1995), suggesting that excessive ethylene inhibits 80

photosynthesis in juvenile leaves. To our knowledge, no actual photosynthesis measurements from 81

non-senescing leaves of Arabidopsis exposed to ethylene are currently available. 82

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

3

The control of photosynthesis by ethylene also affects plant biomass production by influencing final 83

rosette size. Arabidopsis ethylene-insensitive mutants (etr1-1, ein2 and ein3) have larger rosettes 84

compared to wild-type plants (Bleecker et al., 1988; Guzman & Ecker, 1990; Ecker et al., 1995; 85

Alonso et al., 1999). However, this discrepancy is probably manifested during later stages of plant 86

development where ethylene controls photosynthesis by stimulating leaf senescence (Figure 1). 87

Ethylene-insensitive mutants show a delayed onset of senescence, extending their growth period, 88

resulting in larger rosettes compared to wild-type plants (Hua et al., 1995; Grbic and Bleecker, 1995; 89

Alonso et al., 1999; Tholen et al., 2004). Juvenile non-senescing 3-week-old etr1-1 mutants grown in 90

well-ventilated conditions do not have a larger total leaf area and relative growth rate compared to 91

wild type plants during vegetative development despite their reduction in photosynthesis, 92

confirming that delayed senescence in these ethylene-insensitive mutants likely controls rosette size 93

(Tholen et al., 2004). 94

95

Ethylene and chlorophyll content 96

Ethylene can stimulate the degradation of chlorophyll during fruit ripening and leaf senescence 97

(Burg & Burg, 1965; Abeles et al., 1992). In non-senescing developing leaves, ethylene-insensitive 98

mutants (e.g. etr1-1) also have reduced chlorophyll content in Arabidopsis, (Zacarias & Reid, 1990; 99

Grbic & Bleecker, 1995) and protoplasts of etr1-1 have reduced chlorophyll fluorescence (Kim et al., 100

2017), suggesting that basal ethylene levels are required to ensure normal chlorophyll content. The 101

opposite is true for mature leaves prone to senescence, where chlorophyll content is found to be 102

higher in ethylene-insensitive mutants (etr1-1 and ein2-1) of Arabidopsis (Grbic & Bleecker, 1995; Oh 103

et al., 1997), tobacco (Yang et al., 2008) and tomato (Solanum lycopersicum) (Monteiro et al., 2011). 104

Chlorophyll content is also higher in mature leaves of ACC oxidase (ACO) antisense lines of tomato 105

(Picton et al., 1993; John et al., 1995; Jensen & Veierskov, 1998) and ACC synthase (ACS) antisense 106

lines of maize (Zea mays) (Young et al., 2002). These findings suggest that ethylene is involved in 107

establishing normal chlorophyll contents in non-senescing leaves and promotes chlorosis through 108

chlorophyll degradation in mature leaves (Figure 1). 109

Ethylene and stomatal conductance 110

Photosynthesis is intimately linked with stomatal conductance, which mediates CO2 uptake and 111

transpiration (Matthews et al., 2017; Vialet-Chabrand et al., 2017; Males & Griffiths, 2017). Ethylene 112

treatment by ethylene gas, ACC, or ethephon induces stomatal closure in Arabidopsis (Desikan et al., 113

2006). The stomata of Arabidopsis ethylene-insensitive mutants (etr1-1) show reduced conductance 114

compared to wild-type plants (Tholen et al., 2004). These observations suggest that ethylene 115

negatively influences stomatal conductance in Arabidopsis. It must be noted that the etr1-1 mutant 116

also has smaller stomata (Tanaka et al., 2005), indicating that ethylene influences stomatal 117

development. Indeed, Arabidopsis plants continuously grown in ethylene, as well as the constitutive 118

ethylene response mutant ctr1-1, possess more stomata (Kieber et al., 1993), yet it is unknown if 119

these plants also display higher CO2 uptake or net photosynthesis. 120

It is not clear if altered ethylene levels play a primary role on stomatal conductance or have a 121

secondary effect through the crosstalk with abscisic acid (ABA) (Wilkinson & Davies, 2010; Murata et 122

al., 2015). In Arabidopsis, external ethylene, or constitutive internal ethylene production by the 123

eto1-1 mutation, inhibits ABA-induced stomatal closure (Tanaka et al., 2005; Watkins et al., 2014). 124

The ethylene signaling mutants (etr1-1 or ein3-1) and the ethylene perception inhibitor 1-MCP (1-125

methylcyclopropane) do not affect ABA-induced stomatal closure (Tanaka et al., 2005). The 126

inhibition of ABA-induced stomatal closure is also observed in wheat (Triticum aestivum), but older 127

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

4

leaves are more sensitive to ethylene, while younger leaves are more sensitive to ABA (Chen et al., 128

2013). The inhibitory action of ethylene on ABA-induced stomatal closure is mainly regulated by 129

hydrogen peroxide signaling (Desikan, 2005; Desikan et al., 2006; Shi et al., 2015). Ethylene 130

stimulates flavonol production in the guard cells, which subsequently suppresses reactive oxygen 131

species (ROS) accumulation and consequently reduces ABA-induced stomatal closure (Figure 1; 132

Watkins et al., 2014; Watkins et al., 2017). 133

Ethylene and energy dissipation (light reactions) 134

The capture of light energy by photosystems (PS) I and II is necessary to accommodate electron 135

transport and the reduction of CO2 (the so-called dark reactions of photosynthesis) in plant 136

chloroplasts. Wullschleger et al. (1992) re-examined the light-response and CO2-response curves of 137

soybean (Glycine max) reported by Taylor and Gunderson (1988) and found a 30% decline in the 138

electron transport capacity (Jmax) following a 4-hour exposure to ethylene. In line with these results, 139

transient overexpression of a specific ethylene responsive factor (CitERF13) in tobacco leaves 140

compromised photosynthetic rates. Significant declines of the maximum quantum efficiency as well 141

as the effective quantum efficiency of both PS I and II occurred respectively 3 and 2 days after 142

infiltration with Agrobacterium carrying CitERF13 (Xie et al., 2016). In addition, pulse-amplitude 143

modulation fluorimetry-based chlorophyll fluorescence analyses by Kim et al. (2017) reveal that 144

ethylene-insensitive mutants of Arabidopsis (etr1-1) display lower PS II activity compared to wild-145

type plants. These results are further corroborated by augmented expression of the cellular energy 146

stress sensor AKIN10 (ARABIDOPSIS KINASE 10) in ethylene-insensitive mutants. AKIN10 is an 147

isoform of the evolutionarily conserved energy sensor SNF1-RELATED PROTEIN KINASE (SnRK1) and 148

has the ability to modulate the ratio catabolism/anabolism to sustain cellular viability (Broeckx et al., 149

2016). It must be noted that a second mutation in the Arabidopsis etr1-1 mutant produces a 150

premature stop codon in ARC3 (ACCUMULATION AND REPLICATION 3), which is responsible for the 151

abnormally large chloroplasts observed in etr1-1 but not ein2 and ein3 mutants (Cho et al., 2012). 152

ARC3 plays a role in chloroplast division (Maple et al., 2007) and the arc3 mutant displays abnormal 153

chloroplasts in mesophyll protoplasts, independent of the etr1-1 mutation (Cho et al., 2012). Given 154

this important secondary mutation (arc3) in the etr1-1 mutant line commonly used in ethylene 155

research, it is advised to seek additional confirmatory lines of evidence, especially when working on 156

photosynthesis. Nonetheless, ethylene signaling mutants outcrossed from the arc3 secondary 157

mutation (etr1-1sg) are also found to have a lower maximum quantum efficiency, higher chlorophyll 158

fluorescence lifetime of PS II and, consequently, a lower quantum yield of PS II (Kim et al., 2017). 159

These findings suggest that normal ethylene sensitivity is required for optimal photochemical 160

efficiency of PS II independently of an altered chloroplast structure caused by the secondary arc3 161

mutation (Kim et al., 2017). Besides photochemical quenching, ethylene has also been found to 162

influence non-photochemical quenching properties by intervention of the xanthophyll cycle 163

mechanism. Chen and Gallie (2015) demonstrated that Arabidopsis eto1-1 mutants, with increased 164

ethylene production, are affected in their ability to convert violaxanthin to zeaxanthin by impairing 165

violaxanthin de-epoxidase activity. As a consequence, these plants are particularly prone to elevated 166

ROS production and photosensitivity. 167

Ethylene and carbon fixation (dark reactions) and carbohydrate partitioning 168

A study by Grbic & Bleecker (1995) showed that young leaves of Arabidopsis ethylene-insensitive 169 mutants (etr1-1) have reduced Rubisco activity, while older leaves have higher rubisco activity 170 compared to wild type plants. Using ethylene-insensitive transgenic tobacco plants, Tholen et al. 171 (2007) also revealed a decrease in Rubisco transcripts and protein content of about 76% and 42%, 172 respectively, in comparison to wild-type plants. A high degree of downregulation of Rubisco occurs 173 for both ethylene-insensitive tobacco and Arabidopsis seedlings growing on a glucose-enriched 174

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

5

medium (Zhou et al., 1998). Further investigations into the decreased rates of photosynthesis in 175 tobacco after transient overexpression of CitERF13 reveal that the maximum rate of Rubisco 176 carboxylase activity (Vc, max) is indeed affected (Xie et al., 2016). We can conclude from these reports 177 that normal ethylene sensitivity is required to achieve maximal Rubisco activity in non-senescing 178 leaves. As Rubisco is inefficient due to its typical error-prone catalytic properties (Bracher et al., 179 2017), ethylene is also likely to influence protein abundance and/or activity of Rubisco activases 180 (RCAs), adding an additional layer of complexity to mediating the carboxylation process. RCAs are 181 well known as molecular chaperones for Rubisco to deal with its dead-end inhibited complexes due 182 to its high affinity for its substrate ribulose 1,5-bisphosphate and similar sugars when the active site 183 has been left unprimed with CO2 and Mg2+ cofactors (Parry et al., 2008). 184 Khan (2005) reported an increased activity of carbonic anhydrase (CA) in mustard (Brassica juncea) 185 upon a treatment with the ethylene-releasing growth regulator ethephon. Besides participating in 186 the regulatory network to control chloroplast pH and protect stroma enzymes from denaturation 187 during severe and sudden changes in light conditions, CA can elevate the concentration of CO2 in 188 close proximity to rubisco and, as such, limit the proportion of photorespiration (Badger, 2003). 189 Carbonic anhydrase also plays a role in C3 but even more critically in C4 and CAM photosynthesis, 190 providing sufficient bicarbonate to fuel PEPC (DiMario et al., 2017). Work on the effect of ethylene 191 on carbon fixation in C4 and CAM plants is limited. Young et al. (2004) reported that an acs6 192 mutation in maize (C4) results in lower ethylene production, leading to higher Rubisco content and 193 higher CO2 assimilation for both young and mature leaves. These results suggest that basal levels of 194 ethylene suppress maximal carbon fixation in maize. We have not found other studies that report 195 the effect of ethylene on Rubisco, CA nor PEPC in other C4 or CAM plants, making it difficult to draw 196 firm conclusions about the impact of ethylene on C4 and CAM carboxylation. 197 Following diurnal synthesis, triose phosphates need to be continuously removed from the Calvin 198

cycle, by either being deployed for starch formation in the chloroplast or exported to the cytosol to 199

fuel sucrose synthesis to replenish non-photosynthetic parts of the plant. Efficient sucrose transport 200

is critical for achieving optimal carbohydrate partitioning in a plant that is robust but also responsive 201

to environmental changes. To carefully monitor the carbohydrate and energy status, plants use an 202

intricate network of transporters, enzymes and metabolites such as sucrose, glucose, triose, and 203

hexose monophosphates, trehalose-6-phosphate, fructose 1,6 bisphosphate, and fructose 2,6 204

bisphosphate (Braun et al., 2014). It is expected that ethylene also intervenes in carbohydrate 205

partitioning, as different nodes have already been established in the complex webs that interrelate 206

sugar and hormone signaling (Figure 1). The mutually antagonistic relationship between glucose and 207

ethylene signaling confers a nice example (Figure 1; Zhou et al., 1998; León and Sheen, 2003). 208

Ethylene-insensitive plants (etr1, ein2 and ein3) are hypersensitive to glucose (supplemented to the 209

medium), while constitutive ethylene activation (ctr1 mutant) or ethylene overproduction (by eto 210

mutants or ACC treatment) result in decreased sugar sensitivity (León and Sheen, 2003; Zhou et al., 211

1998; Yanagisawa et al., 2003). Conversely, glucose also crosstalks with ethylene by stimulating EIN3 212

degradation, which reduces ethylene sensitivity, causing a feedback mechanism that amplifies 213

glucose sensitivity (Yanagisawa et al., 2003). Moreover, in the rubber tree (Hevea brasiliensis), 214

increased latex production after ethylene treatment is accompanied by the enhanced transcript 215

abundance of HbSUT1A and HbSUT2A, which encode transporters belonging to the SUT (sucrose 216

transporter) group (Dusotoit-Coucaud et al., 2009). More recently, Zhou et al. (2017) also reported 217

altered expression of the TREHALOSE-6-PHOSPHATE SYNTHASE genes (HbTPS1 and HbTPS2) upon 218

ethylene treatment in the rubber tree. In addition, ethylene has recently been shown to accelerate 219

the circadian oscillator to shorten the circadian period, a response that can be overturned by 220

externally applied sucrose (Haydon et al., 2017). These findings indicate that ethylene and the pool 221

of sucrose originating from photosynthesis can crosstalk to influence circadian rhythms and control 222

plant photosynthetic capacity (Haydon et al., 2017). 223

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

6

Ethylene and leaf senescence 224

Besides influencing photosynthesis in non-senescing leaves, ethylene also inhibits photosynthesis 225

through the initiation and stimulation of senescence in mature leaves (Figure 1; Kim et al., 2015). It 226

has been shown that external ethylene stimulates leaf senescence (Bleecker et al., 1988; Zacarias & 227

Reid, 1990), while ethylene-insensitive mutants (etr1-1, ers1, ein2-1, ein2-5, ein3-1 and ein3-1 eil1-1 228

in Arabidopsis and Nr in tomato) show a reduced rate of senescence (Bleecker, 1988; Hua et al., 229

1995; Grbic and Bleecker, 1995; Oh et al., 1997; Lanahan et al., 1994, Li et al., 2013; Kim et al., 2014). 230

Both etr1-1 and ein2-1 mutants have increased ethylene production compared to wild-type plants 231

(Guzman & Ecker, 1990; Woeste et al., 1999), yet their insensitivity towards ethylene overturns the 232

additional ethylene, resulting in a delay in leaf senescence. Eventually, ethylene-insensitive mutants 233

age and show senescence, suggesting that ethylene controls both the rate and timing of leaf 234

senescence (Grbic & Bleecker, 1995). Delayed senescence and concomitant decline in chlorophyll 235

content and photosynthesis has also been observed in antisense plants for ACO of tomato (Picton et 236

al., 1993; John et al., 1995; Jensen & Veierskov, 1998) and acs6 mutants of the C4 plant maize 237

(Young et al., 2004), but not for acs mutants of Arabidopsis (Tsuchisaka et al., 2009). Arabidopsis 238

plants continuously exposed to ethylene gas do not display an enhanced rate of senescence (Kieber 239

et al., 1993), but have smaller rosettes, similar to ethylene overproducing and constitutive ethylene 240

sensitive mutants (eto1-1, eto1-13, ctr1-1; Guzaman & Ecker, 1990; Kieber et al., 1993; Christians et 241

al., 2009). Tomato plants constitutively overexpressing ACS also show altered leaf development but 242

no signs of enhanced senescence (Lanahan et al., 1994). In general, we conclude that a temporal 243

exposure to ethylene stimulates leaf senescence in mature leaves, while continuous exposure 244

instead causes altered leaf development. 245

A transient ethylene treatment of mature leaves stimulates senescence by upregulating the 246

expression of senescence-associated genes (SAGs) (Grbic & Bleecker, 1995; Guo et al., 2004; Breeze 247

et al., 2011; Figure 1). Several important SAGs have been shown to play a prominent role in different 248

cellular processes such as programmed cell death, autophagy, chlorophyll catabolism, plastid 249

differentiation, sugar metabolism, and resource allocation (Thomas, 2012; Pujol, 2015). The master 250

transcription factor EIN3 has been identified as an important player in controlling SAGs (Li et al., 251

2013). It can activate the expression of NAP (NAM/ATAF1,2/CUC2) and NAC2 (ORE1/NAC092), two 252

important transcription factors controlling leaf senescence (Woo et al., 2004; Kim et al., 2009; Kim et 253

al., 2014). Furthermore, EIN3 binds to the promotor of the microRNA (miRNA) miR164 and 254

progressively inhibits its expression during leaf development (Li et al., 2013). In turn, miR164 inhibits 255

the expression of the transcription factor NAC2 (Kim et al., 2009; Kim et al., 2014; Li et al., 2013), 256

unraveling a dual feed-forward and feedback regulation of senescence by ethylene through the 257

action of EIN3 (Figure 1). 258

Ethylene exerts a species specific response on photosynthesis 259

Extensive literature review indicates that the negative effects of ethylene on different aspects of 260

photosynthesis for both juvenile non-senescing and mature senescing leaves cannot be generalized 261

across species. Various physiological experiments with different ethylene treatments have revealed 262

a species-specific reduction in photosynthesis in some plants (including important crops), although 263

ethylene has no effect on photosynthesis in other species (Table 1; Pallas & Kays, 1982; Squier et al., 264

1985; Taylor & Gunderson, 1986) In one mustard species (Brassica juncea) ethylene was found to 265

stimulate photosynthesis (Kahn, 2004; Iqbal et al., 2011). Besides the major crops listed in Table 1, 266

ethylene also lowers photosynthesis in other species such as radish (Raphanus sativus), pumpkin 267

(Cucurbita pepo), green foxtail (Setaria viridis), sweet potato (Ipomoea batatas), sunflower 268

(Helianthus annuus), Jerusalem artichoke (Helianthus tuberosus), common cocklebur (Xanthium 269

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

7

strumarium), and green ash (Fraxinus pennsylvanica), although ethylene has no significant effect on 270

runner bean (Phaseolus coccineus), common orache (Atriplex patula), touch-me-not (Mimosa 271

pudica) and white clover (Trifolium repens) (Pallas & Kays, 1982; Squier et al., 1985; Taylor & 272

Gunderson, 1986; Woodrow et al., 1989). When investigating these data, it should be noted that 273

differences in treatments, growth conditions, timing of the measurements and/or the 274

developmental stage make it impossible to draw firm conclusions, but the general trend is that 275

ethylene inhibits photosynthesis in non-senescing leaves, or has no effect at all on photosynthesis, 276

with the exception of the Brassica juncea species of mustard. Furthermore, studies on tomato and 277

potato (Solanum tuberosum) have shown that a long term ethylene treatment (several days) and its 278

subsequent recovery phase result in a biphasic response of photosynthesis with alternating periods 279

of improved and attenuated photosynthesis compared to the untreated control (Briede et al., 1992; 280

Dueck et al., 2003). These studies provide preliminary insight into the dynamic temporal regulation 281

of photosynthesis by ethylene in tomato and potato, and stress the importance of the time point of 282

sampling after the treatment. In addition, Woodrow et al. (1989) and Woodrow & Grodzinski (1989) 283

provide evidence that the ethylene-induced reduction of photosynthesis in tomato and common 284

cocklebur is mainly caused by a reduced light perception of leaves as a consequence of the epinastic 285

response induced by ethylene. The orientation of the leaves towards the light source is another 286

important element that influences net photosynthesis. 287

Table 1 and the summary above clearly indicate that our knowledge concerning the influences of 288

ethylene on photosynthesis is mainly derived from C3 species. Whilst several C3 plants are listed, 289

with the exception of maize and green foxtail, C4 plants are unrepresented. C4 photosynthesis in 290

maize seems unaffected by an ethylene treatment (Pallaghy & Raschke, 1972; Taylor & Gunderson, 291

1986; Squier et al., 1985), while natural transposon mutants of ACS6 of maize show reduced 292

ethylene biosynthesis, resulting in higher chlorophyll and Rubisco contents and higher 293

photosynthesis rates (Young et al., 2004). These data suggest that endogenous levels of basal 294

ethylene seem to suppress maximal photosynthetic activity in maize. There are no reports that 295

describe the effect of ethylene on CAM photosynthesis to our knowledge; one manuscript reports 296

ethylene gassing experiments with the C3/CAM intermediate ice plant (Mesembryanthemum 297

crystallinum), but only in the C3 mode (Hurst et al., 2004). As no nocturnal increase in either malic 298

acid or PEPC transcripts could be observed after treatment with 200 ppb ethylene, Hurst et al. 299

(2004) concluded that ethylene was not involved in signaling of the C3-CAM transition. 300

301

Concluding remarks 302

The vital process of photosynthesis supplies plants with energy and carbohydrates and sustains 303

other life on earth by the production of precious oxygen. Over recent decades, tremendous 304

advancements have been made in our understanding of the process of photosynthesis and its 305

adjacent pathways, yet its hormonal regulation by ethylene remains largely unexplored (see also 306

Outstanding Questions Box). This review highlights that ethylene exerts species-specific regulation 307

on plant photosynthesis where it reduces photosynthesis in some species, and has no effect in other 308

species. It must be noted that ethylene exerts a dual action in which it reduces photosynthesis in 309

young photosynthetically active leaves and inhibits photosynthesis in older leaves by the stimulation 310

of leaf senescence. We have updated the recent findings on how ethylene interferes in different key 311

processes such as chlorophyll biosynthesis, light reactions, stomatal conductance, carboxylation 312

events, carbohydrate partitioning and leaf senescence. The precise mechanisms of how ethylene 313

controls these processes remain only superficially investigated and more research efforts are needed 314

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

8

to create a profound understanding how ethylene controls one of the most vital processes in plants. 315

In the long term, this knowledge should be translated into biotechnological applications that benefit 316

agriculture. 317

318

Acknowledgements 319

J.C. and B.V.d.P. both thank KU Leuven Internal Funds for financial support and the reviewers for 320

their constructive comments. 321

322

Tables 323

Table 1. Overview of studies that investigate the role of ethylene on net photosynthesis and/or stomatal 324

conductance in different crop species. 325

Species Ethylene treatment

Conditions (PAR and CO2) Sample Plant age

Net photosyn-thesis (PN)

Stomatal conductance (g) Reference

Arachis hypogaea

(C3)

1 ppm ethylene

340 µmol.m-2

.s 350 ppm CO2

1st fully

expanded leaf 1-2 months Decrease Decrease Pallas & Kays,

1982 1-21 ppm ethylene

325 µmol.m-2

.s 318 ppm CO2

Whole plant 5-7 weeks Decrease Decrease Squier et al., 1985

Brassica juncea (C3)

1.5 mM ethephon

1050 µmol.m-2

.s 360 ppm CO2

New fully expanded leaf

45 days Increase Increase Khan, 2004

400 ppm ethephon

1008 µmol.m-2

.s CO2 n.s.

New fully expanded leaf

80 days Decrease Decrease Kahn et al., 2008

200 ppm ethephon

680 µmol.m-2

.s CO2 n.s.

New fully expanded leaf

50 days Increase Increase Iqbal et al., 2011

Glycine max (C3)

5.1 ppm ethylene

510 µmol.m-2

.s CO2 n.s.

New fully expanded leaf

3-8 weeks Decrease Decrease Taylor & Gunderson, 1986

10 ppm ethylene

460 µmol.m-2

.s CO2 n.s.

1st leaf pair 2-3 weeks Decrease Decrease Gunderson &

Taylor, 1991 3.5 ppm

ethylene 338 µmol.m

-2.s

350 ppm CO2 1

st leaf pair 2-32 weeks Decrease Decrease Taylor &

Gunderson, 1988 1-21 ppm

ethylene 325 µmol.m

-2.s

318 ppm CO2 Whole plant 5-7 weeks Decrease Decrease Squier et al., 1985

Gossypium hirsutum (C3)

0.28 kg.ha-

1 ethephon Open field New fully

expanded leaf Early season

Decrease Decrease Pettigrew et al., 1992

5.1 ppm ethylene

510 µmol.m-2

.s CO2 n.s.

New fully expanded leaf

3-8 weeks Decrease Decrease Taylor & Gunderson, 1986

Phaseolus vulgaris (C3)

5.1 ppm ethylene

510 µmol.m-2

.s CO2 n.s.

New fully expanded leaf

3-8 weeks Decrease Decrease Taylor & Gunderson, 1986

1 ppm ethylene

340 µmol.m-2

.s 350 ppm CO2

1st fully

expanded leaf 1-2 months No effect - Pallas & Kays,

1982 1500 ppm

ethephon n.s. Greenhouse conditions

5 leaves 3 months - Decrease Vitagliano & Hoad, 1978

Pisum sativum (C3)

1-10.000 ppm ethylene

1500 µmol.m-2

.s 288 ppm CO2

5th

leaf 20-25 days No effect No effect Pallaghy & Raschke, 1972

5.1 ppm ethylene

510 µmol.m-2

.s CO2 n.s.

New fully expanded leaf

3-8 weeks No effect No effect Taylor & Gunderson, 1986

1 ppm ethylene

340 µmol.m-2

.s 350 ppm CO2

1st fully

expanded leaf 1-2 months No effect - Pallas & Kays,

1982 Nicotiana tabacum

(C3)

1-21 ppm ethylene

325 µmol.m-2

.s 318 ppm CO2

Whole plant 5-7 weeks Decrease Decrease Squier et al., 1985

Solanum lycopersicum

(C3)

5.1 ppm ethylene

510 µmol.m-2

.s CO2 n.s.

New fully expanded leaf

3-8 weeks Decrease No effect Taylor & Gunderson, 1986

300 g.m-3

ethephon

800 µmol.m-2

.s 335 ppm CO2

Whole plant 11-12 leaves

Decrease - Woodrow & Grodzinski, 1989

2 mM ethephon

700 µmol.m-2

.s 300 ppm

New fully expanded leaf

11-12 leaves

No effect No effect Woodrow et al., 1988

Solanum tuberosum (C3)

5.1 ppm ethylene

510 µmol.m-2

.s CO2 n.s.

New fully expanded leaf

3-8 weeks No effect Decrease Taylor & Gunderson, 1986

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

9

1 ppm ethylene

340 µmol.m-2

.s 350 ppm CO2

1st fully

expanded leaf 1-2 months No effect - Pallas & Kays,

1982 1-10 ppm

ethylene 1000 µmol.m

-2.s

340 ppm CO2 New fully expanded leaf

3-4 weeks Decrease Decrease Govindarajan & Poovaiah, 1982

5 ppm ethephon

1200 µmol.m-2

.s CO2 n.s.

1st fully

expanded leaf 30 cm tall plants

Biphasic Increase Briede et al., 1992

450 ppb ethylene

Open field conditions

Whole plant 3.5 weeks Decrease Decrease Dueck et al., 2003

Triticum aestivum

(C3)

5.1 ppm ethylene

510 µmol.m-2

.s CO2 n.s.

New fully expanded leaf

3-8 weeks No effect Decrease Taylor & Gunderson, 1986

50 mM ethephon

1200 µmol.m-2

.s Open field CO2

Flag leaf Flowering plants

No effect Increase Yang et al., 2014

Zea mays (C4)

1-10.000 ppm ethylene

1500 µmol.m-2

.s 288 ppm CO2

5th

leaf 20-25 days No effect No effect Pallaghy & Raschke, 1972

5.1 ppm ethylene

510 µmol.m-2

.s CO2 n.s.

New fully expanded leaf

3-8 weeks No effect No effect Taylor & Gunderson, 1986

1-21 ppm ethylene

325 µmol.m-2

.s 318 ppm CO2

Whole plant 5-7 weeks - No effect Squier et al., 1985

n.s.: not specified; 326

327

Figure legends 328

Figure 1. Overview of the regulatory effects of ethylene on plant photosynthesis and its features for 329 juvenile/non-senescing and mature/senescing leaves. Because the regulation of photosynthesis is species-330 specific, this general scheme does not apply to every species, but merely reflects the general mode of action 331 for the inhibitory effect of ethylene on photosynthesis as found in Arabidopsis. ABA, abscisic acid; CTR1, 332 CONSTITUTIVE TRIPLE RESPONSE 1; EIN2, ETHYLENE INSENSITIVE 2; EIN3, ETHYLENE INSENSITIVE 3; EIL, EIN3-333 LIKE; ERF, ethylene response factors; ETR, ethylene receptor; H2O2, hydrogen peroxide; PAG, 334 photosynthetically active genes; ROS, reactive oxygen species; SAG, senescence-associated gene. 335

Figure 2. Overview of the three modes of photosynthesis (C3, C4 and CAM) in plants, indicating the importance 336 of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and phosphoenolpyruvate carboxylase (PEPC) 337 as main enzymes involved in carbon fixation. 338

Figure 3. Overview of the plant ethylene signal transduction pathway. Ethylene binds the ethylene receptors 339

(ETR) at the endoplasmic reticulum (ER) resulting in auto-phosphorylation of the receptor and inactivation of 340

the downstream kinase CONSTITUTIVE TRIPLE RESPONSE 1 (CTR1). In the absence of ethylene CTR1 341

phosphorylates the ER localized ETHYLENE INSENSITIVE 2 (EIN2) directing it for proteasomal degradation by 342

the ETPs. When ethylene is present, the EIN2 C-terminal part (EIN2-C) is not phosphorylated and gets cleaved 343

and migrates to the nucleus, where it activates the master transcription factor ETHYLENE INSENSITIVE 3 (EIN3) 344

and EIN3-likes (EILs). In the absence of ethylene, EIN3 and EILs are targeted for proteasomal degradation by 345

the ETHYLENE BINDING FACTOR (EBF). EIN3 and EILs on their turn activate ethylene response factors (ERFs) or 346

ethylene responsive genes. The EIN2-C can also interact with the mRNA of selected transcripts, including the 347

5’UTR of the EBF mRNA, to inhibit translation. 348

349

Literature cited 350

Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plants. Academic Press Inc, San Diego, USA. ISBN 351 9780120414512. 352

Adams DO, Yang SF (1977) Methionine metabolism in apple tissue – implication of S-adenosylmethionine as an 353 intermediate in conversion of methionine to ethylene. Plant Physiology 60: 892–896. 354

Adams DO, Yang SF (1979). Ethylene biosynthesis – identification of 1-aminocyclopropane-1-carboxylic acid as 355 an intermediate in the conversion of methionine to ethylene. Proceedings of the National Academy of 356 Sciences U.S.A. 76: 170–174. 357

Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker, JR (1999) EIN2, a Bifunctional Transducer of Ethylene 358 and Stress Responses in Arabidopsis. Science, 284: 2148–2152. 359

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

10

An F, Zhao Q, Ji Y, Li W, Jiang Z, Yu X, Zhang C, Han Y, He W, Liu Y, Zhang S, Ecker JR, Guo H (2010) Ethylene-360 Induced Stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 Is Mediated by Proteasomal Degradation of 361 EIN3 Binding F-Box 1 and 2 That Requires EIN2 in Arabidopsis. The Plant Cell, 22: 2384–2401. 362

Baars C (2017) Review of plant evolution and its effect on climate during the time of the Old Red Sandstone. 363 Proceedings of the Geologists' Association 128(3): 431-437. 364

Badger M (2003) The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. 365 Photosynthesis Research 77: 83e94. 366

Bakshi A, Wilson RL, Lacey RF, Kim H, Wuppalapati SK, Binder BM (2015) Identification of Regions in the 367 Receiver Domain of the ETHYLENE RESPONSE1 Ethylene Receptor of Arabidopsis Important for Functional 368 Divergence. Plant Physiology 169(1): 219–232. 369

Bari R, Jones JDG (2009) Role of plant hormones in plant defense responses. Plant Molecular Biology 69: 473-370 488. 371

Bisson MMA, Groth G (2010). New insight in ethylene signaling: autokinase activity of ETR1 modulates the 372 interaction of receptors and EIN2. Molecular Plant 3: 882–889. 373

Bleecker AB, Estelle MA, Somerville C, Kende H (1988) Insensitivity to ethylene conferred by a dominant 374 mutation in Arabidopsis thaliana. Science 241: 1086–1089. 375

Boller T, Herner RC, Kende H (1979) Assay for and enzymatic formation of an ethylene precursor, 1-376 aminocyclopropane-1-carboxylic acid. Planta 145: 293–303. 377

Borland A, Barrera Zambrano V, Ceusters J, Shorrock K (2011) The photosynthetic plasticity of crassulacean 378 acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New 379 Phytologist, 191(3): 619-633. 380

Braun DM, Wang L, Ruan Y-L (2014) Understanding and manipulating sucrose phloem loading, unloading, 381 metabolism, and signalling to enhance crop yield and food security. Journal of Experimental Botany 65: 1713-382 1735. 383

Breeze E1, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, Zhang C, 384 Morris K, Jenner C, Jackson S, Thomas B, Tabrett A, Legaie R, Moore JD, Wild DL, Ott S, Rand D, Beynon J, 385 Denby K, Mead A, Buchanan-Wollaston V (2011) High-Resolution Temporal Profiling of Transcripts during 386 Arabidopsis Leaf Senescence Reveals a Distinct Chronology of Processes and Regulation. The Plant Cell 23(3): 387 873–894. 388

Briedé J, Fisher JT, Manuchia DJ (1992) Ethephon-mediated Changes in Gas Exchange of Tomato Plants. 389 HortScience 27: 233–235. 390

Bracher A, Whitney SM, Hartl FU, Hayer-Hartl M (2017) Biogenesis and metabolic maintenance of Rubisco. 391 Annual Review of Plant Biology 68: 29-60. 392

Broeckx T, Hulsmans S, Rolland F (2016) The plant energy sensor: evolutionary conservation and divergence of 393 SnRK1 structure, regulation, and function. Journal of Experimental Botany 67: 6215-6252. 394

Burg SG, Burg EA (1965) Ethylene action and the ripening of fruits. Science 148: 1190-1196. 395 Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene response gene ETR1: similarity of 396

product to two-component regulators. Science 262: 539–244. 397 Chang KN1, Zhong S, Weirauch MT, Hon G, Pelizzola M, Li H, Huang SS, Schmitz RJ, Urich MA, Kuo D, Nery JR, 398

Qiao H, Yang A, Jamali A, Chen H, Ideker T, Ren B, Bar-Joseph Z, Hughes TR, Ecker JR (2013) Temporal 399 transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. eLife 400 2013(2): 1–20. 401

Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1998) Activation of the Ethylene Gas 402 Response Pathway in Arabidopsis by the Nuclear Protein ETHYLENE-INSENSITIVE3 and Related Proteins. 403 Cell89: 1133-1144. 404

Chen YF, Randlett MD, Findell JL, Schaller GE (2002) Localization of the ethylene receptor ETR1 to the 405 endoplasmic reticulum of Arabidopsis. The Journal of Biological Chemistry 277: 19861–19866. 406

Chen L, Dodd IC, Davies WJ, Wilkinson S (2013) Ethylene limits abscisic acid- or soil drying-induced stomatal 407 closure in aged wheat leaves. Plant, Cell and Environment, 36(10): 1850-1859. 408

Chen Z, Gallie DR (2015) Ethylene regulates energy-dependent non-photochemical quenching in Arabidopsis 409 through repression of the xanthophyll cycle. PLoS ONE 10(12): e0144209. 410

Cho Y-H, Kim G-D, Yoo S-D (2012) Giant Chloroplast Development in ethylene response1-1 Is Caused by a 411 Second Mutation in ACCUMULATION AND REPLICATION OF CHLOROPLAST3 in Arabidopsis. Molecules and 412 Cells 33: 99-103. 413

Christians MJ, Gingerich DJ, Hansen M, Binder BM, Kieber JJ, Vierstra RD (2009) The BTB ubiquitin ligases ETO1, 414 EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC 415 synthase levels. Plant Journal 57: 332-345. 416

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

11

Desikan R (2005) A Role for ETR1 in Hydrogen Peroxide Signaling in Stomatal Guard Cells. Plant Physiology 417 137(3): 831–834. 418

Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-419 induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant 420 Journal 47(6): 907-16. 421

DiMario RJ, Clayton H, Mukherjee A, Ludwig M, Moroney JV (2017) Plant carbonic anhydrases: structures, 422 locations, evolution, and physiological roles. Molecular Plant 10: 30-46. 423

Dueck TA, Van Dijk CJ, Grashoff C, Groenwold J, Schapendonk AHCM, Tonneijck AEG (2003) Response of potato 424 to discontinuous exposures of atmospheric ethylene: Results of a long-term experiment in open-top 425 chambers and crop growth modelling. Atmospheric Environment 37(12): 1645–1654. 426

Dusotoit-Coucaud A, Brunel N, Kongsawadworakul P, Viboonjun U, Lacointe A, Julien J-L, Chrestin H, Sakr S 427 (2009) Sucrose importation into laticifers of Hevea brasiliensis, in relation to ethylene stimulation of latex 428 production. Annals of Botany 104(4): 635-647. 429

Ecker JR (1995). The ethylene signal transduction pathway in plants. Science 268: 667-675. 430 Gagne JM, Smalle J, Gingerich DJ, Walker JM, Yoo SD, Yanagisawa S, Vierstra RD (2004) Arabidopsis EIN3-431

binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by 432 directing EIN3 degradation. Proceedings of the National Academy of Sciences USA 101: 6803–6808. 433

Govindarajan AG, Poovaiah BW (1982) Effect of root zone carbon dioxide enrichment on ethylene inhibition of 434 carbon assimilation in potato plants. Physiologia Plantarum 55: 465-469. 435

Grbic V, Bleecker AB (1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. The Plant Journal 436 8(4): 595–602. 437

Gunderson CA, Taylor GE (1991) Ethylene Directly Inhibits Foliar Gas Exchange in Glycine max. Plant Physiology 438 95: 337-339. 439

Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCF (EBF1/EBF2)-dependent 440 proteolysis of EIN3 transcription factor. Cell 115: 667–677. 441

Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant, Cell and Environment 27(5): 442 521–549. 443

Guzman P, Ecker JR (1990) Exploiting the Triple Response of Arabidopsis to identify ethylene-related mutants. 444 The Plant Cell 2: 513–523. 445

Haydon MJ, Mielczarek O, Frank A, Roman A, Webb AAR (2017). Sucrose and Ethylene Signaling Interact to 446 Modulate the Circadian Clock. Plant Physiology 175: 947-958. 447

Hua J, Chang C, Sun Q, Meyerowitz E (1995) Ethylene insensitivity conferred by Arabidopsis ERS gene. Science: 448 269: 1712–1714. 449

Hurst AC, Grams TEE, Ratajczak R (2004) Effects of salinity, high irradiance, ozone, and ethylene on mode of 450 photosynthesis, oxidative stress and oxidative damage in the C3/CAM intermediate plant 451 Mesembryanthemum crystallinum L. Plant, Cell and Environment 27: 187-197. 452

Iqbal N, Nazar R, Syeed S, Masood A, Khan NA (2011) Exogenously-sourced ethylene increases stomatal 453 conductance, photosynthesis, and growth under optimal and deficient nitrogen fertilization in mustard. 454 Journal of Experimental Botany 62(14): 4955–4963. 455

Jensen EB, Veierskov B (1998) Interaction between photoperiod, photosynthesis and ethylene formation in 456 tomato plants (Lycopersicon esculentum cv. Ailsa Craig and ACC-oxidase antisense pTOM13). Physiologia 457 Plantarum 103: 363–368. 458

John I, Drake R IA F, Cooper W, Lee P, Horton P, Grierson D (1995) Delayed leaf senescence in ethylene-459 deficient ACC-oxidase antisense tomato plants : molecular and physiological analysis. The Plant Journal: 460 483–490. 461

Ju C, Mee G, Marie J, Lin DY, Ying ZI, Chang J, Garrett WM, Kessenbrock M, Groth G, Tucker ML, Cooper B, 462 Kieber JJ, Chang C (2012) CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone 463 signaling from the ER membrane to the nucleus in Arabidopsis. Proceedings of the National Academy of 464 Sciences USA, 109(47): 19486-91 DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1214848109 465

Ju C, Van de Poel B, Cooper ED, Thierer JH, Gibbons TR, Delwiche CF, Chang C (2015) Conservation of ethylene 466 as a plant hormone over 450 million years of evolution. Nature Plants 1(1): 1–7. 467

Kays SJ, Pallas JE (1980) Inhibition of photosynthesis by ethylene. Nature 285: 51-52. 468 Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends in Plant Science, 469

20(4): 219–229. 470 Khan NA (2004) An evaluation of the effects of exogenous ethephon, an ethylene releasing compound, on 471

photosynthesis of mustard (Brassica juncea) cultivars that differ in photosynthetic capacity. BMC Plant 472 Biology 4: 21. 473

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

12

Khan NA (2005) The influence of exogenous ethylene on growth and photosynthesis of mustard (Brassica 474 juncea) following defoliation. Scientia Horticulturae 105: 499-505. 475

Khan NA, Mir MR, Nazar R, Singh, S (2008) The application of ethephon (an ethylene releaser) increases 476 growth, photosynthesis and nitrogen accumulation in mustard (Brassica juncea L.) under high nitrogen levels. 477 Plant Biology 10(5): 534–538. 478

Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993). CTRI , a Negative Regulator of the Ethylene 479 Pathway in Arabidopsis, Encodes a Member of the Raf Family of Protein Kinases. Cell 72(3): 427–441. 480

Kim G-D, Cho Y-H, Yoo S-D (2017) Phytohormone ethylene-responsive Arabidopsis organ growth under light is 481 in the fine regulation of Photosystem II deficiency-inducible AKIN10 expression. Scientific Reports, 7(1): 2767. 482

Kim HJ, Hong SH, Kim YW, Lee IH, Jun JH, Phee BK, Rupak T, Jeong H, Lee Y, Hong BS, Nam HG, Woo HR, Lim PO 483 (2014). Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-484 INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis. Journal of Experimental Botany 65(14): 485 4023–4036. 486

Kim J, Chang C, Tucker ML (2015) To grow old: regulatory role of ethylene and jasmonic acid in senescence. 487 Frontiers in Plant Science 6: 1–7. 488

Kim J, Woo H, Kim J, Lim P, Lee I, Choi S, Hwang D, Nam HG (2009) Trifurcate Feed-Forward Regulation of Age-489 Dependent Cell Death Involving miR164 in Arabidopsis. Science 490

Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ (1994). The Never Ripe Mutation Blocks Ethylene Perception in 491 Tomato. The Plant Cell 6: 521-530. 492

León P, Sheen J (2003) Sugar and hormone connections. Trends in Plant Science 8(3): 110–116. 493 Li W, Ma M, Feng Y, Li H, Wang Y, Ma Y, Li M, An F, Guo H (2015) EIN2-directed translational regulation of 494

ethylene signaling in Arabidopsis. Cell 163: 670–683. 495 Li Z, Peng J, Wen X, Guo H (2013) ETHYLENE-INSENSITIVE3 Is a Senescence-Associated Gene That Accelerates 496

Age-Dependent Leaf Senescence by Directly Repressing miR164 Transcription in Arabidopsis. The Plant Cell 497 25(9): 3311–3328. 498

Males J, Griffiths H (2017). Stomatal biology of CAM plants. Plant Physiology 174: 550-560. 499 Maple J, Vojta L, Soll J, Moller SG (2007) ARC3 is a stromal Z-ring accessory protein essential for plastid 500

division. EMBO Reports 8: 296–299. 501 Matthews JS, Vialet-Chabrand SR, Lawson T (2017) Diurnal variation in gas exchange: the balance between 502

carbon fixation and water loss. Plant Physiology 174: 614-623. 503 Merchante C, Brumos J, Yun J, Qiwen Hu, Spencer KR, Enríquez P, Binder BM, Heber S, Stepanova AN, Alonso 504

JM (2015) Gene-Specific Translation Regulation Mediated by by the Hormone-Signaling Molecule EIN2. Cell, 505 163: 684–697. 506

Merchante C, Stepanova AN (2017). The triple response assay and its use to characterize ethylene mutants in 507 Arabidopsis. In: Methods in Molecular Biology 1573 - Ethylene Signaling. Eds. Binder BM & Schaller GE. 508 Springer Science. p 163-209. ISBN 978-1-4939-6852-7. 509

Monteiro CC, Carvalho RF, Gratão PL, Carvalho G, Tezotto T, Medici LO, Peres LEP, Azevedo RA (2011) 510 Biochemical responses of the ethylene-insensitive Never ripe tomato mutant subjected to cadmium and 511 sodium stresses. Environmental and Experimental Botany 71(2): 306–320. 512

Moussatche P, Klee HJ (2004) Autophosphorylation activity of the Arabidopsis ethylene receptor multigene 513 family. The Journal of Biological Chemistry 279: 48734–48741. 514

Murata Y, Mori IC, Munemasa S (2015) Diverse Stomatal Signaling and the Signal Integration Mechanism. 515 Annual Review of Plant Biology 66(1): 369–392. 516

Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely 517 nonoverlapping transcriptional responses. Cell 126: 467–475. 518

Oh SA, Park JH, Lee GL, Pack KH, Park SK, Nam HG (1997) Identification of three genetic loci controlling leaf 519 senescence in Arabidopsis thaliana. Plant Journal 12: 527–535. 520

Pallaghy CK, Raschke K (1972). No Stomatal Response to Ethylene. Plant Physiology 49: 275-276. 521 Pallas JE, Kays SJ (1982). Inhibition of Photosynthesis by Ethylene-A Stomatal Effect. Plant Physiology 70: 598-522

601. 523 Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an 524

EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in 525 tobacco. The Plant Cell 13(5): 1035–1046. 526

Parry MAJ, Keys AJ, Madgwick PJ, Carmo-Silva AE, Andralojc PJ (2008) Rubisco regulation: a role for inhibitors. 527 Journal of Experimental Botany 59: 1569-1580 528

Pettigrew WT, Heitholt JJ, Meredith WRJ (1992) Early season ethephon application effects on cotton 529 photosynthesis. Agronomy Journal 85: 821-825. 530

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

13

Picton S, Barton SL, Bouzayen M, Hamilton AJ, Grierson D (1993). Altered fruit ripening and leaf senescence in 531 tomatoes expressing an antisense ethylene-forming enzyme transgene. The Plant Journal 3: 469–481. 532

Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent 533 regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115: 534 679–689. 535

Pujol B (2015) Genes and quantitative genetic variation involved with senescence in cells, organs, and the 536 whole plant. Frontiers in Plant Science 6: 57. 537

Qiao H, Shen Z, Huang SC, Schmitz RJ, Urich MA, Briggs SP, Ecker JR (2012) Processing and subcellular 538 trafficking of ER tethered EIN2 control response to ethylene gas. Science 338:390–393. 539

Qiao H, Chang KN, Yazaki J, Ecker JR (2009) Interplay between ethylene, ETP1/ETP2 F-box proteins, and 540 degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes and Development 23(4): 512–521. 541

Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker R (1995) Genetic Analysis of Ethylene Signal Transduction 542 in Arabidopsis thaliana: Five Novel Mutant Loci Integrated into a Stress Response Pathway. Genetics: 139, 543 1393–1409. 544

Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and evolution of C4 photosynthesis. Annual Review of 545 Plant Biology 63: 19-47. 546

Schaller GE, Ladd NA, Lanahan MB, Spanbauer MJ, Bleecker AB (1995) The ethylene response mediator ETR1 547 from Arabidopsis forms a disulfide-linked dimer. Journal of Biological Chemistry 270(21): 12526–12530. 548

Shi C, Qi C, Ren H, Huang A, Hei S, She X (2015) Ethylene mediates brassinosteroid-induced stomatal closure 549 via G protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis. Plant Journal 82(2): 550 280–301. 551

Solano R, Stepanova A, Chao Q, Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene 552 signaling : a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-553 FACTOR1. Genes and Development 12: 3703–3714. 554

Squier SA, Taylor GE, Selvidge WJ, Gunderson CA (1985) Effect of ethylene and related hydrocarbons on carbon 555 assimilation and transpiration in herbaceous and woody species. Environmental Science and Technology, 556 19(5): 432–437. 557

Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N (2005) Ethylene Inhibits Abscisic Acid-Induced Stomatal 558 Closure in Arabidopsis. Plant Physiology: 138, 2337–2343. 559

Taylor GE, Gunderson CA (1988) Physiological Site of Ethylene Effects on Carbon Dioxide. Plant Physiology 86: 560 85–92. 561

Tholen D, Pons TL, Voesenek L.ACJ, Poorter H (2007) Ethylene insensitivity results in down-regulation of 562 Rubisco expression and photosynthetic capacity in Tobacco. Plant Physiology 144: 1305-15. 563

Tholen D, Pons TL, Voesenek LACJ, Poorter H (2008) The role of ethylene perception in the control of 564 photosynthesis. Plant Signaling & Behavior 3(2): 108–109. 565

Tholen D, Voesenek L ACJ, Poorter H (2004). Ethylene insensitivity does not increase leaf area or relative 566 growth rate in Arabidopsis, Nicotiana tabacum, and Petunia x hybrida. Plant Physiology 134(4): 1803–12. 567

Thomas H (2013) Senescence, ageing and death of the whole plant. New Phytologist 197: 696-711. 568 Tsuchisaka A, Yu G, Jin H, Alonso JM, Ecker JR, Zhang X, Gao S, Theologis A (2009) A combinatorial interplay 569

among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis 570 thaliana. Genetics 183(3): 979–1003. 571

Van de Poel B, Smet D, Van Der Straeten D (2015) Ethylene and Hormonal Cross Talk in Vegetative Growth and 572 Development. Plant Physiology 169: 61–72. 573

Van de Poel B, Cooper ED, Van Der Straeten D, Chang D, Delwiche CF (2016). Transcriptome Profiling of the 574 Green Alga Spirogyra pratensis (Charophyta) Suggests an Ancestral Role for Ethylene in Cell Wall Metabolism, 575 Photosynthesis, and Abiotic Stress Responses. Plant Physiology 172: 533-545. 576

Ververidis P, John P (1991) Complete recovery in vitro of ethylene-forming enzyme-activity. Phytochemistry 577 30: 725–727. 578

Vialet-Chabrand SR, Matthews JS, McAusland L, Blatt MR, Griffiths H, Lawson T (2017). Temporal dynamics of 579 stomatal behaviour: modelling,and implications for photosynthesis and water use. Plant Physiology 174: 603-580 613. 581

Vitagliano C, Hoad GV (1978). Leaf stomatal resistance, ethylene evolution and ABA levels as influenced by (2-582 chloroethyl) phosphonic acid. Scientia Horticulturae 8(2): 101–106. 583

Watkins JM, Hechler PJ, Muday GK (2014) Ethylene-Induced Flavonol Accumulation in Guard Cells Suppresses 584 Reactive Oxygen Species and Moderates Stomatal Aperture. Plant Physiology 164: 1707-1717. 585

Watkins JM, Chapman JM, Muday GK (2017) Abscisic acid-induced reactive oxygen species are modulated by 586 flavonols to control stomata aperature. Plant Physiology 175: 1807-1825. 587

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

14

Wen X, Zhang C, Ji Y, Zhao Q, He W, An F, Jiang L, Guo H (2012) Activation of ethylene signaling is mediated by 588 nuclear translocation of the cleaved EIN2 carboxyl terminus. Cell Research 22: 1613–1616. 589

Wen C (2015). Ethylene in Plants. Springer, Amsterdam, The Netherlands. ISBN 9789401794848. 590 West-Eberhard MJ, Smith JAC, Winter K (2011) Photosynthesis, reorganized. Science 332:311-312. 591 Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to 592

community. Plant, Cell and Environment, 33(4): 510–525. 593 Woeste KE, Ye C, Kieber JJ (1999) Two Arabidopsis Mutants That Overproduce Ethylene Are Affected in the 594

Posttranscriptional Regulation of 1-Aminocyclopropane-1-Carboxylic Acid Synthase. Plant Physiology: 119, 595 521–529. 596

Woo HR, Kim JH, Nam HG, Lim PO (2004) The Delayed Leaf Senescence Mutants of Arabidopsis, ore1, ore3, 597 and ore9 are Tolerant to Oxidative Stress. Plant Cell & Physiology 45: 923-932. 598

Woodrow L, Grodzinski B (1989). An evaluation of the effects of ethylene on carbon assimilation in 599 lycopersicon esculentum. Journal of Experimental Botany 40: 361–368. 600

Woodrow L, Jiao J, Tsujita MJ, Grodzinski B (1989). Whole Plant and Leaf Steady State Gas Exchange during 601 Ethylene Exposure in Xanthium strumarium L. Plant Physiology 90(1): 85–90. 602

Woodrow L, Thompson RG, Grodzinski B (1988). Effects of ethylene on photosynthesis and partitioning in 603 tomato, Lycopersicon esculentum Mill. Journal of Experimental Botany 39(6): 667–684. 604

Wullschleger SD, Hanson PJ, Gunderson CA (1992) Assessing the influence of exogenous ethylene on electron 605 transport and fluorescence quenching in leaves of Glycine max. Environmental and Experimental Botany 32: 606 449-455. 607

Xie X, Xia X, Kuang S, Zhang X, Yin X (2017) Plant Science A novel ethylene responsive factor CitERF13 plays a 608 role in photosynthesis regulation. Plant Science 256: 112–119. 609

Yanagisawa S, Yoo S-D, Sheen J (2003). Differential regulation of EIN3 stability by glucose and ethylene 610 signaling in plants. Nature 425: 521–525. 611

Yang TF, Gonzalez-Carranza ZH, Maunders MJ, Roberts JA (2008) Ethylene and the Regulation of Senescence 612 Processes in Transgenic Nicotiana sylvestris Plants. Annals of Botany 101: 301-310. 613

Yang W, Yin Y, Jiang W, Peng D, Yang D, Cui Y, Wang Z (2014) Severe water deficit-induced ethylene production 614 decreases photosynthesis and photochemical efficiency in flag leaves of wheat. Photosynthetica 52(3): 341–615 350. 616

Young TE, Meeley RB, Gallie DR (2004) ACC synthase expression regulates leaf performance and drought 617 tolerance in maize. Plant Journal 40(5): 813–825. 618

Zacarias L, Reid MS (1990) Role of growth regulators in the senescence of Arabidopsis thaliana leaves. 619 Physiologia Plantarum 80: 549–554. 620

Zhou L, Jang J, Jones T, Sheen J (1998) Glucose and ethylene signal transduction crosstalk revealed by an 621 Arabidopsis glucose-insensitive mutant. Proceedings of the National Academy of Sciences USA 95: 10294-622 10299. 623

Zhou BH, Fang YJ, Fan YJ, Wang Y, Qi JY, Tang CR (2017) Expressional characterization of two class I trehalose-624 6-phosphate synthase genes in Hevea brasiliensis (para rubber tree) suggests a role in rubber production. 625 New Forests 48: 513-526. 626

627

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

Juvenile/non-senescing leaves Mature/senescing leaves

ETR

CTR1

Ethylene

EIN2

EIN3/EILs

ERFs

PAG

PS I & II efficiency

Chlorophyll contentETR

CTR1

Ethylene

EIN2

EIN3/EILs

ERFs

SAG

Chlorophyll catabolism

Stress

Photosynthesis Photosynthesis

ABA

Flavonols

Stomatal closureROS (H2O2)

Chlorophyll biosynthesis

miR164

Glucose/sugars

Sugar partitioning

Rubisco

Figure 1. General overview of the regulatory effects of ethylene on plant photosynthesis and

sub-elements that are likely to co-regulate photosynthesis for both juvenile/non-senescing and

mature/senescing leaves. Because the regulation of photosynthesis is species-specific, this gen-

eral scheme does not apply to every species (e.g. ethylene stimulates photosynthesis in mus-

tard), but merely reflects the general mode of action for the inhibitory effect of ethylene on

photosynthesis. ABA, Abscisic acid; CTR1, CONSTITUTIVE TRIPPLE RESPONSE 1; EIN2, ETHYLENE

INSENSITIVE 2; EIN3, ETHYLENE INSENSITIVE 3; EILs, EIN3-likes; ERF, ethylene response factors;

ETR, ethylene receptor; PAG, photosynthetically active genes; ROS, reactive oxygen species; SAG,

senescence associated genes.

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

C3 plants C4 plants CAM plants

Calvin

cycle

Glyceraldehyde

3-phosphate

CO2

Mesophyll

cell

Calvin

cycle

CO2

Bundle

sheath

cell

Malic acid (C4)Mesophyll

cell

CO2

CO2

Calvin

cycle

CO2

Malic acid (C4)

Mesophyll

cell

CO2

Night

Day

Rubisco

PEPC PEPC

Rubisco Rubisco

Glyceraldehyde

3-phosphate

Glyceraldehyde

3-phosphate

Sucrose Sucrose Sucrose

Figure 2. Simplified overview of the three modes of photo-

synthesis (C3, C4 and CAM) in plants, indicating the impor-

tance of ribulose-1,5-bisphosphate carboxylase/oxygenase

(Rubisco) and phosphoenolpyruvate carboxylase (PEPC) as

main enzymes involved in carbon fixation.

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

P P

P

P P

P

CH

HC

H

H

ETREIN2

CTR1

ETP

EIN3EIN3

EBF

EIN2-C

ERFs

ER

Nucleus

ER lumen

Cytosol

NO ETHYLENE ETHYLENE

EBF

Ethylene responsive genes

EBF mRNA

EIN2-C

EIN2

CTR1

ETRC

H

HC

H

H

CH

HC

H

H

CH

HC

H

H

Figure 3. General overview of the plant ethylene signaling transduction pathway. Ethylene binds with the

ethylene receptors (ETR) at the endoplasmic reticulum (ER) resulting in auto-phosphorylation of the receptor

and inactivation of the downstream kinase CONSTITUTIVE TRIPPLE RESPONSE 1 (CTR1). In the absence of

ethylene CTR1 phosphorylates the ER localized ETHYLENE INSENSITIVE 2 (EIN2) directing it for proteasomal

degradation by the ETPs. When ethylene is present, the EIN2 C-terminal part (EIN2-C) is not phosphorylated

and gets cleaved and migrates to the nucleus, where it activates the master transcription factor ETHYLENE

INSENSITIVE 3 (EIN3) and EIN3-likes (EILs). In the absence of ethylene, EIN3 and EILs are readily targeted for

proteasomal degradation by the ETHYLENE BINDING FACTOR (EBF). EIN3 and EILs on their turn activate

ethylene response factors (ERFs) or ethylene responsive genes. The EIN2-C can also interact with the mRNA of

selected transcripts, including the 5’UTR of the EBF mRNA, to inhibit translation.

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

BOX 1. Photosynthetic Pathways in Plants

Photosynthesis involves the light-mediated conversion of inorganic substrates (i.e. carbon dioxide and water) into organic compounds and occurs via three pathways in terrestrial plants (Fig. 2). C3 is the ancient and most common pathway, found in about 93% of plant species. C3 photosynthesis relies on direct CO2 fixation during the light period in the chloroplasts, mediated by the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). C4 and crassulacean acid metabolism (CAM) can be regarded as evolutionary adaptive mechanisms of photosynthesis that enhance the CO2 concentration at the Rubisco carboxylation site, thus helping plants adapt to the pronounced reduction in CO2 and rise in O2 levels that started about 350 million years ago (Baars, 2017). Both modes of photosynthesis deploy the same machinery present in C3 plants, but differ in the initial mode of carboxylation (West-Eberhard et al., 2011). Carbon uptake in C4 plants (about 1% of plant species) uses diurnal activity of phosphoenolpyruvate carboxylase (PEPC) in the leaf mesophyll cells followed by decarboxylation of the synthesized malic acid in the chloroplasts of bundle sheath cells where Rubisco activity is enhanced by achieving high internal CO2 concentrations (Sage et al., 2012). CAM plants (about 6% of plant species) employ a temporal separation between carboxylation events, allowing initial nocturnal CO2 sequestration by PEPC followed by Rubisco-mediated carboxylation during daytime behind closed stomata, thereby conserving considerable amounts of water (Borland et al., 2011).

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

BOX 2. Ethylene Biosynthesis and Signaling in

Plants

Ethylene is a gaseous hormone that can easily migrate from cell to cell, gradually diffusing throughout the tissue and regulating ethylene-responsive processes (Fig. 3). Most of the ethylene signaling pathway was unraveled by screening for ethylene-related mutants in dark-grown seedlings (triple response) of Arabidopsis (Merchante and Stepanova, 2017). In the light, these mutants have different phenotypes, such as altered photosynthesis. Screening for light-specific ethylene mutants can provide new insights into how ethylene regulates photosynthesis. Ethylene is produced from the precursor 1-aminocyclopropane-1-carboxylic acid (ACC; Adams and Yang, 1979) by the dioxygenase ACC-oxidase (ACO; Ververidis and John, 1991). ACC is synthesized from S-adenosyl-L-methionine by ACC-synthase (ACS; Adams and Yang, 1977; Boller et al., 1979). The synthesized ethylene can bind to the ethylene receptor (Bleecker et al., 1988), a two-component receptor kinase (Chang et al., 1993) located at the endoplasmic reticulum (ER; Chen et al., 2002) forming active hetero- and homodimers (Schaller et al., 1995; Bakshi et al., 2015). Ethylene binding to the active site promotes autophosphorylation of the receptor (Moussatche and Klee, 2004; Bisson and Groth, 2010) and inactivation of the downstream kinase CONSTITUTIVE TRIPLE RESPONSE1 (CTR1; Kieber et al., 1993). Active CTR1 kinase phosphorylates

ETHYLENE INSENSITIVE2 (EIN2; Ju et al., 2012), an ER-bound N-ramp protein (Alonso et al., 1999), which is subsequently targeted for proteasomal degradation by two F-box proteins, EIN2 TARGETING PROTEIN1 (ETP1) and ETP2 (Qiao et al., 2009). When ethylene is bound to its receptor, EIN2 is not phosphorylated and gets cleaved by an unknown protease (Qiao et al., 2012). After cleavage, the EIN2 C-terminal fragment migrates to the nucleus (Ju et al., 2012; Qiao et al., 2012; Wen et al., 2012). There, the C-terminal end activates the master transcription factor EIN3 (Roman et al., 1995; Chao et al., 1998) and its homologs EIN3-LIKE1-3 (EIL1-3) (Chao et al., 1998). In the absence of ethylene, EIN3 and EILs are rapidly turned over by proteasomal degradation through the action of two F-box proteins ETHYLENE BINDING FACTOR1 (EBF1) and EBF2 (Guo and Ecker, 2003; Potuschak et al., 2003; Gagne et al., 2004; An et al., 2010). Recent work also demonstrated that the EIN2 C-terminal end inhibits translation of the EBFs through interaction with their 5′UTR mRNA region, which blocks ribosomal activity (Merchante et al., 2015; Li et al., 2015). Activated EIN3 and EILs bind to an ethylene binding sequence in ethylene-responsive genes, of which the ETHYLENE RESPONSIVE FACTORS (Solano et al., 1998) encode downstream secondary transcription factors that induce ethylene-responsive gene expression (Nemhouser et al., 2006; Chang et al., 2013).

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

ADVANCES

• Integrating available surveys of different plant species reveals a species-specific regulation of photosynthesis by ethylene. Ethylene inhibits photosynthesis in some plants, but not in others, and was found to stimulate photosynthesis in only mustard (Brassica juncea).

• Ethylene interacts with photosynthesis at different mechanistic levels by influencing transcription, translation, and key enzyme activities implicated in chlorophyll synthesis, stomatal conductance, light capture, electron transport, carbon fixation, and carbohydrate partitioning.

• Ethylene cross talks with sugar metabolism to fine tune feedback mechanisms of photosynthesis.

• The ethylene master transcription factors EIN3/EIL control SAG genes and senescence-associated microRNAs in senescing leaves as well as PAG genes in juvenile leaves.

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

OUTSTANDING QUESTIONS

• Why is the action of ethylene on photosynthesis species-specific? Other ethylene-regulated processes are also species-specific, such as hyponasty, epinasty, aerenchyma formation, climacteric fruit ripening, etc., but we lack a comprehensive physiological explanation.

• What are the downstream ethylene-responsive transcription factors that control photosynthesis-related gene expression?

• What is the effect of ethylene on the initial carboxylation mediated by CA and PEPC in C4 and CAM plants?

• How does ethylene influence carbohydrate partitioning in photosynthesizing leaves?

• Ethylene triggers leaf senescence and thus reduces photosynthesis in an age-dependent manner. What are developmental cues that control this age-dependent regulatory role of ethylene on leaf senescence?

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

Parsed CitationsAbeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plants. Academic Press Inc, San Diego, USA. ISBN 9780120414512.

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

Adams DO, Yang SF (1977) Methionine metabolism in apple tissue – implication of S-adenosylmethionine as an intermediate inconversion of methionine to ethylene. Plant Physiology 60: 892–896.

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

Adams DO, Yang SF (1979). Ethylene biosynthesis – identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in theconversion of methionine to ethylene. Proceedings of the National Academy of Sciences U.S.A. 76: 170–174.

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

Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker, JR (1999) EIN2, a Bifunctional Transducer of Ethylene and Stress Responsesin Arabidopsis. Science, 284: 2148–2152.

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

An F, Zhao Q, Ji Y, Li W, Jiang Z, Yu X, Zhang C, Han Y, He W, Liu Y, Zhang S, Ecker JR, Guo H (2010) Ethylene-Induced Stabilization ofETHYLENE INSENSITIVE3 and EIN3-LIKE1 Is Mediated by Proteasomal Degradation of EIN3 Binding F-Box 1 and 2 That Requires EIN2in Arabidopsis. The Plant Cell, 22: 2384–2401.

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

Baars C (2017) Review of plant evolution and its effect on climate during the time of the Old Red Sandstone. Proceedings of theGeologists' Association 128(3): 431-437.

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

Badger M (2003) The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. Photosynthesis Research 77:83e94.

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

Bakshi A, Wilson RL, Lacey RF, Kim H, Wuppalapati SK, Binder BM (2015) Identification of Regions in the Receiver Domain of theETHYLENE RESPONSE1 Ethylene Receptor of Arabidopsis Important for Functional Divergence. Plant Physiology 169(1): 219–232.

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

Bari R, Jones JDG (2009) Role of plant hormones in plant defense responses. Plant Molecular Biology 69: 473-488.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Bisson MMA, Groth G (2010). New insight in ethylene signaling: autokinase activity of ETR1 modulates the interaction of receptors andEIN2. Molecular Plant 3: 882–889.

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

Bleecker AB, Estelle MA, Somerville C, Kende H (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsisthaliana. Science 241: 1086–1089.

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

Boller T, Herner RC, Kende H (1979) Assay for and enzymatic formation of an ethylene precursor, 1-aminocyclopropane-1-carboxylicacid. Planta 145: 293–303.

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

Borland A, Barrera Zambrano V, Ceusters J, Shorrock K (2011) The photosynthetic plasticity of crassulacean acid metabolism: an www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from

Copyright © 2018 American Society of Plant Biologists. All rights reserved.

evolutionary innovation for sustainable productivity in a changing world. New Phytologist, 191(3): 619-633.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Braun DM, Wang L, Ruan Y-L (2014) Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling toenhance crop yield and food security. Journal of Experimental Botany 65: 1713-1735.

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

Breeze E1, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, Zhang C, Morris K, JennerC, Jackson S, Thomas B, Tabrett A, Legaie R, Moore JD, Wild DL, Ott S, Rand D, Beynon J, Denby K, Mead A, Buchanan-Wollaston V(2011) High-Resolution Temporal Profiling of Transcripts during Arabidopsis Leaf Senescence Reveals a Distinct Chronology ofProcesses and Regulation. The Plant Cell 23(3): 873–894.

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

Briedé J, Fisher JT, Manuchia DJ (1992) Ethephon-mediated Changes in Gas Exchange of Tomato Plants. HortScience 27: 233–235.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Bracher A, Whitney SM, Hartl FU, Hayer-Hartl M (2017) Biogenesis and metabolic maintenance of Rubisco. Annual Review of PlantBiology 68: 29-60.

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

Broeckx T, Hulsmans S, Rolland F (2016) The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure,regulation, and function. Journal of Experimental Botany 67: 6215-6252.

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

Burg SG, Burg EA (1965) Ethylene action and the ripening of fruits. Science 148: 1190-1196.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene response gene ETR1: similarity of product to two-component regulators. Science 262: 539–244.

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

Chang KN1, Zhong S, Weirauch MT, Hon G, Pelizzola M, Li H, Huang SS, Schmitz RJ, Urich MA, Kuo D, Nery JR, Qiao H, Yang A, JamaliA, Chen H, Ideker T, Ren B, Bar-Joseph Z, Hughes TR, Ecker JR (2013) Temporal transcriptional response to ethylene gas drivesgrowth hormone cross-regulation in Arabidopsis. eLife 2013(2): 1–20.

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

Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1998) Activation of the Ethylene Gas Response Pathway inArabidopsis by the Nuclear Protein ETHYLENE-INSENSITIVE3 and Related Proteins. Cell89: 1133-1144.

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

Chen YF, Randlett MD, Findell JL, Schaller GE (2002) Localization of the ethylene receptor ETR1 to the endoplasmic reticulum ofArabidopsis. The Journal of Biological Chemistry 277: 19861–19866.

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

Chen L, Dodd IC, Davies WJ, Wilkinson S (2013) Ethylene limits abscisic acid- or soil drying-induced stomatal closure in aged wheatleaves. Plant, Cell and Environment, 36(10): 1850-1859.

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

Chen Z, Gallie DR (2015) Ethylene regulates energy-dependent non-photochemical quenching in Arabidopsis through repression ofthe xanthophyll cycle. PLoS ONE 10(12): e0144209.

Pubmed: Author and Title www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Cho Y-H, Kim G-D, Yoo S-D (2012) Giant Chloroplast Development in ethylene response1-1 Is Caused by a Second Mutation inACCUMULATION AND REPLICATION OF CHLOROPLAST3 in Arabidopsis. Molecules and Cells 33: 99-103.

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

Christians MJ, Gingerich DJ, Hansen M, Binder BM, Kieber JJ, Vierstra RD (2009) The BTB ubiquitin ligases ETO1, EOL1 and EOL2act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant Journal 57: 332-345.

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

Desikan R (2005) A Role for ETR1 in Hydrogen Peroxide Signaling in Stomatal Guard Cells. Plant Physiology 137(3): 831–834.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closurein Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant Journal 47(6): 907-16.

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

DiMario RJ, Clayton H, Mukherjee A, Ludwig M, Moroney JV (2017) Plant carbonic anhydrases: structures, locations, evolution, andphysiological roles. Molecular Plant 10: 30-46.

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

Dueck TA, Van Dijk CJ, Grashoff C, Groenwold J, Schapendonk AHCM, Tonneijck AEG (2003) Response of potato to discontinuousexposures of atmospheric ethylene: Results of a long-term experiment in open-top chambers and crop growth modelling. AtmosphericEnvironment 37(12): 1645–1654.

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

Dusotoit-Coucaud A, Brunel N, Kongsawadworakul P, Viboonjun U, Lacointe A, Julien J-L, Chrestin H, Sakr S (2009) Sucroseimportation into laticifers of Hevea brasiliensis, in relation to ethylene stimulation of latex production. Annals of Botany 104(4): 635-647.

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

Ecker JR (1995). The ethylene signal transduction pathway in plants. Science 268: 667-675.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Gagne JM, Smalle J, Gingerich DJ, Walker JM, Yoo SD, Yanagisawa S, Vierstra RD (2004) Arabidopsis EIN3-binding F-box 1 and 2 formubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proceedings of the NationalAcademy of Sciences USA 101: 6803–6808.

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

Govindarajan AG, Poovaiah BW (1982) Effect of root zone carbon dioxide enrichment on ethylene inhibition of carbon assimilation inpotato plants. Physiologia Plantarum 55: 465-469.

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

Grbic V, Bleecker AB (1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. The Plant Journal 8(4): 595–602.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Gunderson CA, Taylor GE (1991) Ethylene Directly Inhibits Foliar Gas Exchange in Glycine max. Plant Physiology 95: 337-339.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCF (EBF1/EBF2)-dependent proteolysis of EIN3transcription factor. Cell 115: 667–677.

Pubmed: Author and Title www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant, Cell and Environment 27(5): 521–549.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Guzman P, Ecker JR (1990) Exploiting the Triple Response of Arabidopsis to identify ethylene-related mutants. The Plant Cell 2: 513–523.

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

Haydon MJ, Mielczarek O, Frank A, Roman A, Webb AAR (2017). Sucrose and Ethylene Signaling Interact to Modulate the CircadianClock. Plant Physiology 175: 947-958.

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

Hua J, Chang C, Sun Q, Meyerowitz E (1995) Ethylene insensitivity conferred by Arabidopsis ERS gene. Science: 269: 1712–1714.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Hurst AC, Grams TEE, Ratajczak R (2004) Effects of salinity, high irradiance, ozone, and ethylene on mode of photosynthesis, oxidativestress and oxidative damage in the C3/CAM intermediate plant Mesembryanthemum crystallinum L. Plant, Cell and Environment 27:187-197.

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

Iqbal N, Nazar R, Syeed S, Masood A, Khan NA (2011) Exogenously-sourced ethylene increases stomatal conductance, photosynthesis,and growth under optimal and deficient nitrogen fertilization in mustard. Journal of Experimental Botany 62(14): 4955–4963.

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

Jensen EB, Veierskov B (1998) Interaction between photoperiod, photosynthesis and ethylene formation in tomato plants(Lycopersicon esculentum cv. Ailsa Craig and ACC-oxidase antisense pTOM13). Physiologia Plantarum 103: 363–368.

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

John I, Drake R IA F, Cooper W, Lee P, Horton P, Grierson D (1995) Delayed leaf senescence in ethylene-deficient ACC-oxidaseantisense tomato plants : molecular and physiological analysis. The Plant Journal: 483–490.

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

Ju C, Mee G, Marie J, Lin DY, Ying ZI, Chang J, Garrett WM, Kessenbrock M, Groth G, Tucker ML, Cooper B, Kieber JJ, Chang C (2012)CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus inArabidopsis. Proceedings of the National Academy of Sciences USA, 109(47): 19486-91DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1214848109

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

Ju C, Van de Poel B, Cooper ED, Thierer JH, Gibbons TR, Delwiche CF, Chang C (2015) Conservation of ethylene as a plant hormoneover 450 million years of evolution. Nature Plants 1(1): 1–7.

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

Kays SJ, Pallas JE (1980) Inhibition of photosynthesis by ethylene. Nature 285: 51-52.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends in Plant Science, 20(4): 219–229.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Khan NA (2004) An evaluation of the effects of exogenous ethephon, an ethylene releasing compound, on photosynthesis of mustard(Brassica juncea) cultivars that differ in photosynthetic capacity. BMC Plant Biology 4: 21. www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from

Copyright © 2018 American Society of Plant Biologists. All rights reserved.

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

Khan NA (2005) The influence of exogenous ethylene on growth and photosynthesis of mustard (Brassica juncea) following defoliation.Scientia Horticulturae 105: 499-505.

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

Khan NA, Mir MR, Nazar R, Singh, S (2008) The application of ethephon (an ethylene releaser) increases growth, photosynthesis andnitrogen accumulation in mustard (Brassica juncea L.) under high nitrogen levels. Plant Biology 10(5): 534–538.

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

Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993). CTRI , a Negative Regulator of the Ethylene Pathway inArabidopsis, Encodes a Member of the Raf Family of Protein Kinases. Cell 72(3): 427–441.

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

Kim G-D, Cho Y-H, Yoo S-D (2017) Phytohormone ethylene-responsive Arabidopsis organ growth under light is in the fine regulation ofPhotosystem II deficiency-inducible AKIN10 expression. Scientific Reports, 7(1): 2767.

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

Kim HJ, Hong SH, Kim YW, Lee IH, Jun JH, Phee BK, Rupak T, Jeong H, Lee Y, Hong BS, Nam HG, Woo HR, Lim PO (2014). Generegulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leafsenescence signalling in Arabidopsis. Journal of Experimental Botany 65(14): 4023–4036.

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

Kim J, Chang C, Tucker ML (2015) To grow old: regulatory role of ethylene and jasmonic acid in senescence. Frontiers in Plant Science6: 1–7.

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

Kim J, Woo H, Kim J, Lim P, Lee I, Choi S, Hwang D, Nam HG (2009) Trifurcate Feed-Forward Regulation of Age-Dependent Cell DeathInvolving miR164 in Arabidopsis. Science

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

Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ (1994). The Never Ripe Mutation Blocks Ethylene Perception in Tomato. The Plant Cell6: 521-530.

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

León P, Sheen J (2003) Sugar and hormone connections. Trends in Plant Science 8(3): 110–116.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Li W, Ma M, Feng Y, Li H, Wang Y, Ma Y, Li M, An F, Guo H (2015) EIN2-directed translational regulation of ethylene signaling inArabidopsis. Cell 163: 670–683.

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

Li Z, Peng J, Wen X, Guo H (2013) ETHYLENE-INSENSITIVE3 Is a Senescence-Associated Gene That Accelerates Age-Dependent LeafSenescence by Directly Repressing miR164 Transcription in Arabidopsis. The Plant Cell 25(9): 3311–3328.

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

Males J, Griffiths H (2017). Stomatal biology of CAM plants. Plant Physiology 174: 550-560.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Maple J, Vojta L, Soll J, Moller SG (2007) ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Reports 8: www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

Maple J, Vojta L, Soll J, Moller SG (2007) ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Reports 8:296–299.

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

Matthews JS, Vialet-Chabrand SR, Lawson T (2017) Diurnal variation in gas exchange: the balance between carbon fixation and waterloss. Plant Physiology 174: 614-623.

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

Merchante C, Brumos J, Yun J, Qiwen Hu, Spencer KR, Enríquez P, Binder BM, Heber S, Stepanova AN, Alonso JM (2015) Gene-Specific Translation Regulation Mediated by by the Hormone-Signaling Molecule EIN2. Cell, 163: 684–697.

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

Merchante C, Stepanova AN (2017). The triple response assay and its use to characterize ethylene mutants in Arabidopsis. In: Methodsin Molecular Biology 1573 - Ethylene Signaling. Eds. Binder BM & Schaller GE. Springer Science. p 163-209. ISBN 978-1-4939-6852-7.

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

Monteiro CC, Carvalho RF, Gratão PL, Carvalho G, Tezotto T, Medici LO, Peres LEP, Azevedo RA (2011) Biochemical responses of theethylene-insensitive Never ripe tomato mutant subjected to cadmium and sodium stresses. Environmental and Experimental Botany71(2): 306–320.

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

Moussatche P, Klee HJ (2004) Autophosphorylation activity of the Arabidopsis ethylene receptor multigene family. The Journal ofBiological Chemistry 279: 48734–48741.

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

Murata Y, Mori IC, Munemasa S (2015) Diverse Stomatal Signaling and the Signal Integration Mechanism. Annual Review of PlantBiology 66(1): 369–392.

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

Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlappingtranscriptional responses. Cell 126: 467–475.

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

Oh SA, Park JH, Lee GL, Pack KH, Park SK, Nam HG (1997) Identification of three genetic loci controlling leaf senescence inArabidopsis thaliana. Plant Journal 12: 527–535.

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

Pallaghy CK, Raschke K (1972). No Stomatal Response to Ethylene. Plant Physiology 49: 275-276.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Pallas JE, Kays SJ (1982). Inhibition of Photosynthesis by Ethylene-A Stomatal Effect. Plant Physiology 70: 598-601.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-typetranscription factor enhances resistance against pathogen attack and osmotic stress in tobacco. The Plant Cell 13(5): 1035–1046.

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

Parry MAJ, Keys AJ, Madgwick PJ, Carmo-Silva AE, Andralojc PJ (2008) Rubisco regulation: a role for inhibitors. Journal ofExperimental Botany 59: 1569-1580

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

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

Pettigrew WT, Heitholt JJ, Meredith WRJ (1992) Early season ethephon application effects on cotton photosynthesis. AgronomyJournal 85: 821-825.

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

Picton S, Barton SL, Bouzayen M, Hamilton AJ, Grierson D (1993). Altered fruit ripening and leaf senescence in tomatoes expressingan antisense ethylene-forming enzyme transgene. The Plant Journal 3: 469–481.

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

Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent regulation of plantethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115: 679–689.

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

Pujol B (2015) Genes and quantitative genetic variation involved with senescence in cells, organs, and the whole plant. Frontiers inPlant Science 6: 57.

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

Qiao H, Shen Z, Huang SC, Schmitz RJ, Urich MA, Briggs SP, Ecker JR (2012) Processing and subcellular trafficking of ER tetheredEIN2 control response to ethylene gas. Science 338:390–393.

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

Qiao H, Chang KN, Yazaki J, Ecker JR (2009) Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggersethylene responses in Arabidopsis. Genes and Development 23(4): 512–521.

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

Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker R (1995) Genetic Analysis of Ethylene Signal Transduction in Arabidopsisthaliana: Five Novel Mutant Loci Integrated into a Stress Response Pathway. Genetics: 139, 1393–1409.

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

Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and evolution of C4 photosynthesis. Annual Review of Plant Biology 63: 19-47.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Schaller GE, Ladd NA, Lanahan MB, Spanbauer MJ, Bleecker AB (1995) The ethylene response mediator ETR1 from Arabidopsis formsa disulfide-linked dimer. Journal of Biological Chemistry 270(21): 12526–12530.

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

Shi C, Qi C, Ren H, Huang A, Hei S, She X (2015) Ethylene mediates brassinosteroid-induced stomatal closure via G protein-activatedhydrogen peroxide and nitric oxide production in Arabidopsis. Plant Journal 82(2): 280–301.

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

Solano R, Stepanova A, Chao Q, Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling : atranscriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes and Development 12:3703–3714.

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

Squier SA, Taylor GE, Selvidge WJ, Gunderson CA (1985) Effect of ethylene and related hydrocarbons on carbon assimilation andtranspiration in herbaceous and woody species. Environmental Science and Technology, 19(5): 432–437.

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

Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N (2005) Ethylene Inhibits Abscisic Acid-Induced Stomatal Closure in Arabidopsis.Plant Physiology: 138, 2337–2343.

Pubmed: Author and Title www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Taylor GE, Gunderson CA (1988) Physiological Site of Ethylene Effects on Carbon Dioxide. Plant Physiology 86: 85–92.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Tholen D, Pons TL, Voesenek L.ACJ, Poorter H (2007) Ethylene insensitivity results in down-regulation of Rubisco expression andphotosynthetic capacity in Tobacco. Plant Physiology 144: 1305-15.

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

Tholen D, Pons TL, Voesenek LACJ, Poorter H (2008) The role of ethylene perception in the control of photosynthesis. Plant Signaling& Behavior 3(2): 108–109.

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

Tholen D, Voesenek L ACJ, Poorter H (2004). Ethylene insensitivity does not increase leaf area or relative growth rate in Arabidopsis,Nicotiana tabacum, and Petunia x hybrida. Plant Physiology 134(4): 1803–12.

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

Thomas H (2013) Senescence, ageing and death of the whole plant. New Phytologist 197: 696-711.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Tsuchisaka A, Yu G, Jin H, Alonso JM, Ecker JR, Zhang X, Gao S, Theologis A (2009) A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics 183(3): 979–1003.

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

Van de Poel B, Smet D, Van Der Straeten D (2015) Ethylene and Hormonal Cross Talk in Vegetative Growth and Development. PlantPhysiology 169: 61–72.

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

Van de Poel B, Cooper ED, Van Der Straeten D, Chang D, Delwiche CF (2016). Transcriptome Profiling of the Green Alga Spirogyrapratensis (Charophyta) Suggests an Ancestral Role for Ethylene in Cell Wall Metabolism, Photosynthesis, and Abiotic StressResponses. Plant Physiology 172: 533-545.

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

Ververidis P, John P (1991) Complete recovery in vitro of ethylene-forming enzyme-activity. Phytochemistry 30: 725–727.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Vialet-Chabrand SR, Matthews JS, McAusland L, Blatt MR, Griffiths H, Lawson T (2017). Temporal dynamics of stomatal behaviour:modelling,and implications for photosynthesis and water use. Plant Physiology 174: 603-613.

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

Vitagliano C, Hoad GV (1978). Leaf stomatal resistance, ethylene evolution and ABA levels as influenced by (2-chloroethyl) phosphonicacid. Scientia Horticulturae 8(2): 101–106.

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

Watkins JM, Hechler PJ, Muday GK (2014) Ethylene-Induced Flavonol Accumulation in Guard Cells Suppresses Reactive OxygenSpecies and Moderates Stomatal Aperture. Plant Physiology 164: 1707-1717.

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

Watkins JM, Chapman JM, Muday GK (2017) Abscisic acid-induced reactive oxygen species are modulated by flavonols to controlstomata aperature. Plant Physiology 175: 1807-1825.

Pubmed: Author and Title www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Wen X, Zhang C, Ji Y, Zhao Q, He W, An F, Jiang L, Guo H (2012) Activation of ethylene signaling is mediated by nuclear translocation ofthe cleaved EIN2 carboxyl terminus. Cell Research 22: 1613–1616.

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

Wen C (2015). Ethylene in Plants. Springer, Amsterdam, The Netherlands. ISBN 9789401794848.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

West-Eberhard MJ, Smith JAC, Winter K (2011) Photosynthesis, reorganized. Science 332:311-312.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant, Cell andEnvironment, 33(4): 510–525.

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

Woeste KE, Ye C, Kieber JJ (1999) Two Arabidopsis Mutants That Overproduce Ethylene Are Affected in the PosttranscriptionalRegulation of 1-Aminocyclopropane-1-Carboxylic Acid Synthase. Plant Physiology: 119, 521–529.

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

Woo HR, Kim JH, Nam HG, Lim PO (2004) The Delayed Leaf Senescence Mutants of Arabidopsis, ore1, ore3, and ore9 are Tolerant toOxidative Stress. Plant Cell & Physiology 45: 923-932.

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

Woodrow L, Grodzinski B (1989). An evaluation of the effects of ethylene on carbon assimilation in lycopersicon esculentum. Journal ofExperimental Botany 40: 361–368.

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

Woodrow L, Jiao J, Tsujita MJ, Grodzinski B (1989). Whole Plant and Leaf Steady State Gas Exchange during Ethylene Exposure inXanthium strumarium L. Plant Physiology 90(1): 85–90.

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

Woodrow L, Thompson RG, Grodzinski B (1988). Effects of ethylene on photosynthesis and partitioning in tomato, Lycopersiconesculentum Mill. Journal of Experimental Botany 39(6): 667–684.

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

Wullschleger SD, Hanson PJ, Gunderson CA (1992) Assessing the influence of exogenous ethylene on electron transport andfluorescence quenching in leaves of Glycine max. Environmental and Experimental Botany 32: 449-455.

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

Xie X, Xia X, Kuang S, Zhang X, Yin X (2017) Plant Science A novel ethylene responsive factor CitERF13 plays a role in photosynthesisregulation. Plant Science 256: 112–119.

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

Yanagisawa S, Yoo S-D, Sheen J (2003). Differential regulation of EIN3 stability by glucose and ethylene signaling in plants. Nature 425:521–525.

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

Yang TF, Gonzalez-Carranza ZH, Maunders MJ, Roberts JA (2008) Ethylene and the Regulation of Senescence Processes inTransgenic Nicotiana sylvestris Plants. Annals of Botany 101: 301-310.

Pubmed: Author and Title www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Yang W, Yin Y, Jiang W, Peng D, Yang D, Cui Y, Wang Z (2014) Severe water deficit-induced ethylene production decreasesphotosynthesis and photochemical efficiency in flag leaves of wheat. Photosynthetica 52(3): 341–350.

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

Young TE, Meeley RB, Gallie DR (2004) ACC synthase expression regulates leaf performance and drought tolerance in maize. PlantJournal 40(5): 813–825.

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

Zacarias L, Reid MS (1990) Role of growth regulators in the senescence of Arabidopsis thaliana leaves. Physiologia Plantarum 80: 549–554.

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

Zhou L, Jang J, Jones T, Sheen J (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proceedings of the National Academy of Sciences USA 95: 10294-10299.

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

Zhou BH, Fang YJ, Fan YJ, Wang Y, Qi JY, Tang CR (2017) Expressional characterization of two class I trehalose-6-phosphate synthasegenes in Hevea brasiliensis (para rubber tree) suggests a role in rubber production. New Forests 48: 513-526.

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

www.plantphysiol.orgon March 1, 2019 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.