The Plant Cell, December 2014 © 2014 12/12/2014 The American …€¦ · 20/01/2015 · • Plants get the rest of their nutrients as mineral nutrients • Mineral nutrients are

The Plant Cell, December 2014 © 2014The American Society of Plant Biologists

12/12/2014

www.plantcell.org/cgi/doi/10.1105/tpc.114.tt1214 1

© 2014 American Society of Plant Biologists

Plant Nutrition 2: Macronutrients (N, P, K, S, Mg and Ca)


“Earth, and not water, is the matter that constitutes vegetables”

Woodward, J. (1699). Some thoughts and experiments concerning vegetation.PhilosophicalTransactions of the Royal Society, 21,193-227.

“Some thoughts and experiments concerning

vegetation” (1699)

Spring water

Rainwater

Thames River water

Weight gain:

55% 62% 93%

Woodward concluded that mineral matter nourishes plants, laying the foundation for the study of plant mineral nutrition

Woodward compared plant growth in water containing different amounts of “mineral matter” to test the assumption that water is a plant’s sole requirement


“Law of the Minimum”: Nutrient in least supply limits growth

Biodiversity Heritage Library

Justus von Liebig1803 - 1873

Carl Sprengel1787 - 1859

Growth is determined by whichever nutrient is

present in shortest supply

Stamp issued 150 years after his birth


Lawes & Gilbert began investigating plant nutrition at Rothamsted 1843

Images used by permission of Rothamsted Research

Joseph Henry Gilbert1817 - 1901

John Bennett Lawes1814 - 1901

Lawes’ estate is now Rothamsted Research, the longest-running agricultural experiment station

Lawes’ Superphosphate factory pioneered the production of chemically-synthesized fertilizers


Plants assimilate mineral nutrients from their surroundings

K+

K+

PO43-PO43-

PO43-

NO3-NO3-

K+ K+

K+

K+

K+

K+

PO43-

PO43-

PO43-

NO3-

NO3-

Nutrient assimilation can occur across the surface of the plant or through the root system of vascular plants


Plants assimilate mineral nutrients mainly as cations or anions

μmol / g (dry wt)

Element Assimilated form

250 Potassium (K) K+

1000 Nitrogen (N) NO3‐, NH4+

60 Phosphorus (P)

HPO42‐,H2PO4‐

30 Sulfur (S) SO42‐

80 Magnesium (Mg)

Mg2+

125 Calcium (Ca) Ca2+

μmol / g (dry wt)

Element Assimilated form

2 Iron (Fe) Fe3+, Fe2+

0.002 Nickel (Ni) Ni+

1 Manganese (Mn)

Mn2+

0.1 Copper (Cu) Cu2+

0.001 Molybdenum (Mo)

MoO42+

2 Boron (B) H3BO33 Chlorine (Cl) Cl‐

0.3 Zinc (Zn) Zn2+

MACRONUTRIENTS MICRONUTRIENTS

Charged ions require transport proteins to cross membranes

See Taiz, L. and Zeiger, E. (2010) Plant Physiology. Sinauer Associates; Marschner, P. (2012) Mineral Nutrition of Higher Plants. Academic Press, London


However, larger and more complex nutrients also can be taken up

Schmidt, S., Raven, J.A. and Paungfoo-Lonhienne, C. (2013). The mixotrophic nature of photosynthetic plants. Funct. Plant Biol. 40: 425-438 by permission of CSIRO Publishing; Adlassnig, W., Koller-Peroutka, M., Bauer, S., Koshkin, E., Lendl, T. and Lichtscheidl, I.K. (2012). Endocytotic uptake of nutrients in carnivorous plants. Plant J. 71: 303-313. Hill, P.W., Marsden, K.A. and Jones, D.L. (2013). How significant to plant N nutrition is the direct consumption of soil microbes by roots? New Phytol. 199: 948-955.

Carnivorous plants can obtain nutrients by digesting trapped animals

Other, non-carnivorous plants can obtain nutrients from proteins and even microbes, although these processes are very inefficient


Vascular plants assimilate mineral nutrients mostly via roots

Barberon, M. and Geldner, N. (2014). Radial transport of nutrients: the plant root as a polarized epithelium. Plant Physiol. 166: 528-537.

By increasing surface area for absorption, root hairs functionally resemble microvilli of an animal’s intestinal epithelium

Membrane transporters facilitate nutrient uptake


Roots have several adaptations to enhance nutrient capture

Schmidt, S., Raven, J.A. and Paungfoo-Lonhienne, C. (2013). The mixotrophic nature of photosynthetic plants. Funct. Plant Biol. 40: 425-438 by permission of CSIRO publishing.

Fungal symbiotic partners

Prokaryotic symbiotic

partners

Developmental responses

Biochemical responses


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Nutrient uptake, assimilation and utilization involve many processes

Nutrient uptake

efficiency

Nutrient utilization efficiency

Root system architecture

Root exudates

Rhizosphere microbiota

Symbioses

PP

N N

NH3

Transporters and pumps

Intercellular transport efficiency

X R-XAssimilation and

remobilization efficiency

Regulatory and homeostatic

networks


Soil pH affects nutrient availability-Some soils are acidic, others basic

Atlas of the biosphere, University of Wisconsin; FMoeckel

Strongly acidic

Mildly alkaline


Physical and biological processes affect nutrient availability

Reprinted from Scholes, M.C. and Scholes, R.J. (2013). Dust unto dust. Science. 342: 565-566; See also Tedersoo, L., et al., and Abarenkov, K. (2014). Global diversity and geography of soil fungi. Science. 346: 1256688.

Erosion, rainfall patterns, cultural practices, soil biodiversity, soil pH, atmospheric gases etc. all affect soil fertility


Nutrients removed from soils can be replenished with fertilizers

Total nutrient requirement

Typical fertilizer application

Cor

n

Soy W

heat

Cot

ton

Ric

e

Kg/

haK

g/ha

1000

800

600

400

200

0

0

200

400

Nitrogen

Phosphate

Potash

Magnesium

Sulfur

Most fertilizers contain nitrogen (N), phosphorus (P) and potassium (K). Some include other elements

Fertilizers can be complex waste

products or refined blends of

nutrient salts

Plants remove nutrients from the soil

Source: USGS


Global mineral nutrient resources are unevenly distributed

Supply > Demand

Supply < Demand

FAO (2011) Current world fertilizer trends and outlook to 2015.

NP2O5K2O


The global trade in fertilizers is worth billions of dollars annually

IFIA

Ammonium Urea Potash Diammonium phosphate

Monoammonium phosphate

Phosphate rock

Sulfur Sulfuric acid


How much is the right amount of fertilizer to apply to a field?

Photo by Michael Russelle.

Species / variety of plant: Different plants have different needs

Soil characteristics: Residual nutrients, rate of nutrient leaching, pH, particle size, presence of microbes etc. affect optimal application

Cultivation practices: Is unharvested material removed, or left to replenish the soil?

Abiotic and biotic factors: Temperature, rain, stress and pests or pathogens affect nutrient needs

Developmental stage affects plant needs

Interactions between nutrients: There are both positive and negative interactions between various nutrients

Financial considerations: Balancing the cost of fertilizers with the gain reaped from their use


Fertilizer use can cause environmental and health problems

Nitrogen fixation is energy demanding

Phosphate and potash mining is destructive

Image source: Lamiot; Alexandra Pugachevsky

Transport requires energy

Human and animal waste can spread disease N ON

Nitrous oxide (N2O) derived from fertilizer is a

major greenhouse gas

Nutrient runoff pollutes waterways and can lead

to eutrophication

Plants need nutrients, but their application isn’t always optimal or sustainable – how can plant science contribute to better practices?


Fertilizer use is increasing to keep pace with population growth

Rock weatheringDecaying matterOrganic matterInorganic matter

Fertilizers

Deposition from atmosphere

Vance, C.P. (2001). Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol. 127: 390-397.


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Summary: Overview of plant nutrient requirements and fertilizers

• People eat plants (or eat animals or products from animals that eat plants)

• Plants get C, H and O from water and carbon dioxide• Plants get the rest of their nutrients as mineral nutrients• Mineral nutrients are usually ions in soil solution• Mineral nutrients are taken up across membranes and

moved throughout the plant as needed• The nutrients that plants remove from the soil must be

replenished• Fertilizer use can contribute to environmental problems


Nitrogen: The most abundant mineral element in a plant

• The most abundant element in the earth’s atmosphere

• The 4th most abundant element in a plant (after C, H and O)

• Often the limiting nutrient for plant growth

Nitrogen is one of the three major

macronutrients found in most fertilizers

N is in amino acids (proteins), nucleic acids (DNA, RNA), chlorophyll, and countless small molecules

Blank, L.M. (2012). The cell and P: From cellular function to biotechnological application. Curr. Opin. Biotech. 23: 846 – 851.From: Buchanan, B.B., Gruissem, W. and Jones, R.L. (2000) Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists.


Nitrogen can be found in many inorganic forms

Species Name Oxidation State

R‐NH2 Organic nitrogen, urea ‐3NH3, NH4+ Ammonia,

ammonium ion‐3

N2 Nitrogen 0N2O Nitrous oxide +1NO Nitric oxide +2HNO2, NO2‐ Nitrous acid,

nitrite ion+3

NO2 Nitrogen dioxide +4HNO3, NO3‐ Nitric acid, nitrate ion +5

Adapted from Robertson, G.P. and Vitousek, P.M. (2009). Nitrogen in agriculture: Balancing the cost of an essential resource. Annu. Rev. Environ. Res. 34: 97-125.

NO2-

NO3-

NO2- NON2O

N2

NH3Nitrate

reduction

Nitrogen fixation

Nitrification

Anaerobic reactions

Aerobic reactions


Plants are an important part of the global nitrogen cycle

Atmospheric pool of N2Biological

fixationAtmospheric

fixationIndustrial fixation

NO3-

NH4+NO3-

NH4+

NO3-

NO2- NO3-NH4+

Nitrification by nitrifying bacteria

R-NH2

manure

Assimilation by plants

decomposition

Den

itrifi

catio

n by

de

nitri

fyin

g ba

cter

ia

Biological fixation

(oceans)

120 Tg N / yr(50%

agricultural)

120 Tg N / yr

140Tg N / yr

5 Tg N / yr

Adapted from Fowler, D., et al. (2013). The global nitrogen cycle in the twenty-first century. Phil. Trans. Roy. Soc. B: 368: 20130164


How do plants optimize their uptake and utilization of nitrogen?

How is nitrogen taken up into the plant?

How is inorganic nitrogen assimilated into organic molecules?

How do plants sense local soil nitrogen levels and plant nitrogen status?

How do plants respond to nitrogen deficit? How do they maximize uptake through their roots?

How do plants remobilize nitrogen to optimize N-utilization?


Nitrogen metabolism: Uptake, assimilation and remobilization

Uptake

NO3-

NH4+

NH4+

NO3-

Nitrate reductase

NO2-

Nitrite reductase

Glutamine synthetase

(GS)

Glutamate

GlutamineIncorporation into amino acids and other nitrogen-containing compounds

Amino acid recycling,

photorespiration

Carbon poolsTCA cycle

2-oxoglutarate

Glutamate

Glutamine-2-oxoglutarate

aminotransferase (GOGAT)

AssimilationRemobilization

AssimilationNH4+R-NH2

N2 Adapted from Xu, G., Fan, X. and Miller, A.J. (2012). Plant nitrogen assimilation and use efficiency. Annu. Rev. Plant Biol. 63: 153-182.


Most plants take up most of their nitrogen as nitrate NO3-

See Li, B., Li, G., Kronzucker, H.J., Baluška, F. and Shi, W. (2014). Ammonium stress in Arabidopsis: signaling, genetic loci, and physiological targets. Trends Plant Sci. 19: 107-114; Britto, D.T. and Kronzucker, H.J. (2013). Ecological significance and complexity of N-source preference in plants. Ann. Bot. 112: 957-963.

Nitrate reductase

Nitrite reductase

NO2- NO3-NH4+

Nitrification by nitrifying prokaryotes

Energy released

Energy released

Many prokaryotes oxidize NH4+, so soil NH4+ levels are often low

NO2- NH4+NO3-

Energy consumed

Energy consumed

Plants use energy to reduce NO3- for assimilation into organic compounds

R-NH3

Plant preferences for NH4+ vs NO3- vary by species, other metabolic processes, temperature, water, soil pH etc….


Plants have specific transporters for NO3-, NH4+ and other N forms

Nacry, P., Bouguyon, E. and Gojon, A. (2013). Nitrogen acquisition by roots: physiological and developmental mechanisms ensuringplant adaptation to a fluctuating resource. Plant Soil. 370: 1-29, With kind permission from Springer Science and Business Media

HATS = high affinity transportersLATS = low affinity transporters


A major nitrate importer was the first cloned: CHL1/ NRT1.1/ NPF6.3

Oostindiër-Braaksma, F.J. and Feenstra, W.J. (1973). Isolation and characterization of chlorate-resistant mutants of Arabidopsis thaliana. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis. 19: 175-185; Reprinted from Tsay, Y.-F., Schroeder, J.I., Feldmann, K.A. and Crawford, N.M. (1993). The herbicide sensitivity gene CHL1 of arabidopsis encodes a nitrate-inducible nitrate transporter. Cell. 72: 705-713 with permission from Elsevier.

Chlorate (ClO3-) mimics nitrate (NO3-)

Nitrate reductase

Chlorite ClO2-

Wild-type

Chlorate uptake mutant (chl1-5)

Nitrate reductase

mutant

+ +-

Growth on chlorate

Nitrate reductase activity

The first nitrate transporter was identified using a genetic selection for chlorate resistance

1973In 1993 the CHL1 gene was cloned and found to be a nitrate transporter (shown = current in Xenopus oocytes)


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Other channels contribute to nitrate transport w/in and between cells

Reprinted from Wang, Y.-Y., Hsu, P.-K. and Tsay, Y.-F. (2012). Uptake, allocation and signaling of nitrate. Trends Plant Sci. 17: 458-467 with permission from Elsevier; Tegeder, M. (2014). Transporters involved in source to sink partitioning of amino acids and ureides: opportunities for crop improvement. J. Exp. Bot. 65: 1865-1878 by permission of Oxford University Press.

Specific transporters move nitrate (or other N-containing

compounds) inwards and outwards across the PM and

across the vacuolar membrane

Nitrogen uptake but also assimilation and recycling depend on membrane transporters


Primary N assimilation: NO3- is reduced to NH4+ prior to assimilation

Uptake

NO3-

NH4+

NH4+

NO3-

Nitrate reductase

NO2-

Nitrite reductase


(GS)

Glutamine

Assimilation into organic compounds

All other N-containing compounds

R-NH3

Glutamate


Nitrate reductase is a large enzyme with a complex catalytic scheme

Lambeck, I.C., Fischer-Schrader, K., Niks, D., Roeper, J., Chi, J.-C., Hille, R. and Schwarz, G. (2012). Molecular mechanism of 14-3-3 protein-mediated inhibition of plant nitrate reductase. J. Biol. Chem. 287: 4562-4571.

NO2-NO3-

NADH NAD+

NADHNO3-

Nitrate reductase reduces nitrate to nitrate with NADH acting as the electron donor

The electrons move from NADH to FAD to heme to a molybdenum cofactor (Moco) to NO3-


GS/GOGAT assimilates inorganic nitrogen into organic molecules

NH4+


(GS)

Glutamate



photorespiration


2-oxoglutarate

Glutamate



Assimilation

Remobilization

Uptake


Gln synthetase (GS) expression is regulated by many factors

GS1 (GLN1 genes) Cytosolic protein

GS2 (GLN2 genes) Nuclear gene, plastid localized protein

GS activity is regulated transcriptionally and post-transcriptionally by cell type, light, [NH4+], circadian cycles, plant carbon status etc.

GS activity is correlated with nitrogen use efficiency

Martin, A., et al., and Hirel, B. (2006). Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell. 18: 3252-3274.


Rebmobilization of N occurs during senescence and photorespiration

Avice, J.-C. and Etienne, P. (2014). Leaf senescence and nitrogen remobilization efficiency in oilseed rape (Brassica napus L.). J. Exp. Bot. 65: 3813-3824 by permission of Oxford University Press.

Leaves Roots, CotyledonsAmino acids Amino acids

Glutamate Glutamate

Glutamate GlutamateGlutamine Glutamine

NH4+ NH4+

NADH-GOGATFdx-GOGAT

Chloroplast localized GS2

Cytosolic GS1

Assimilation Assimilation

AA catabolism

Photo-respiration

Each N atom may cycle through GS many times as amino acids are recycled

during growth and senescence and released due to photorespiration

uptake

assimilation

assimilation

remobilization

remobilization


Hirel, B., Le Gouis, J., Ney, B. and Gallais, A. (2007). The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J. Exp. Bot. 58: 2369-2387 by permission of Oxford University Press.

In some plants, most grain N is remobilized from vegetative tissues

The relative amount of N taken up pre- and post-flowering is important in nitrogen use efficiency

Different crop rely more or less on N remobilization from vegetative tissues


Summary: Plant nitrogen uptake and assimilation

Uptake

NO3-

NH4+

NH4+

NO3-

Nitrate reductase

NO2-

Nitrite reductase


(GS)

Glutamate



photorespiration


2-oxoglutarate

Glutamate



AssimilationRemobilization

AssimilationNH4+R-NH2

N2 Adapted from Xu, G., Fan, X. and Miller, A.J. (2012). Plant nitrogen assimilation and use efficiency. Annu. Rev. Plant Biol. 63: 153-182.


Regulation: Nitrogen sensing, signaling and deficit responses

See for example Scheible, W.-R., et al and Stitt, M. (2004). Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 136: 2483-2499; Krapp, A. et al and Daniel-Vedele, F. (2011). Arabidopsis roots and shoots show distinct temporal adaptation patterns toward nitrogen starvation. Plant Physiol. 157: 1255-1282. Schlüter, U., et al. and Sonnewald, U. (2012). Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis. Plant Physiol. 160: 1384-1406. Amiour, N. et al and Hirel, B. (2012). The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. J. Exp. Bot. 63: 5017-5033. Balazadeh, S., et al. and Mueller-Roeber, B. (2014). Reversal of senescence by N resupply to N-starved Arabidopsis thaliana: transcriptomic and metabolomic consequences. J. Exp. Bot. 63: 5017-5033.

NITROGEN DEFICITIncrease uptake

Metabolic adaptations to low-N

Accelerated senescence and nitrogen remobilization

Activation of some NO3- and NH4+ transportersPreferential growth of root relative to shoot

Decreased accumulation of N-rich chlorophyll Increased accumulation N-free anthocyanins Smaller pools of N-containing compounds (amino acids)Larger pools of N-free compounds (starches, organic acids)


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Responses to NO3- can be separated from those to N-metabolites

Wang, R., Tischner, R., Gutiérrez, R.A., Hoffman, M., Xing, X., Chen, M., Coruzzi, G., Crawford, N.M. (2004). Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol. 136: 2512–2522; Canales, J., Moyano, T.C., Villarroel, E. and Gutiérrez, R.A. (2014). Systems analysis of transcriptome data provides new hypotheses about Arabidopsis root response to nitrate treatments. Front. Plant Sci. 5: 22.

Nitrate reductase

Nitrite reductase

NO2- NH4+NO3- R-NH3XNitrate reductase mutants allow responses to NO3-to be separated from responses to N-metabolites

Red indicates nitrate-specificgenes

NR mutant can’t grow on NO3-

Transcriptional responses to nitrate (+ downstream

metabolites)

10% of the genome responds to nitrate, but only some genes are nitrate-specific


CHL1/NRT1.1/NPF6.3 is a nitrate transceptor (sensor)

Remans, T., et al. and Gojon, A. (2006). The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc. Natl. Acad. Sci. 103: 19206-19211 © by the National Academy of Sciences; Krouk, G., et al. and Gojon, A. (2010). Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Devel. Cell. 18: 927-937 with permission from Elsevier.

Lateral roots of transceptor mutants (chl1-10) fail to respond to the HN environment

In wild-type plants (Ws), lateral root growth is stimulated in High Nitrate (HN)

WT

chl1-5

Transceptor mutants (chl1-5) also show

abnormal transcriptional responses to nitrate


Reprinted by permission from Wiley from Drew, M.C. (1975). Comparison of the effects of a localised supply of phosphate, nitrate and ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol. 75: 479-490.. Reprinted from Bouguyon, E., Gojon, A. and Nacry, P. (2012). Nitrate sensing and signaling in plants. Sem. Cell Devel. Biol. 23: 648-654, with permission from Elsevier. See also Gersani, M. and Sachs, T. (1992). Development correlations between roots in heterogeneous environments. Plant Cell Environ. 15: 463-469.

When nitrogen is abundant, plants allocate less biomass to their roots

When nitrogen distribution is patchy, roots proliferate in the nutrient rich patches

Roots respond to local and systemic nitrogen availability


The split-root system separates local and systemic signals

All plants split with ½ root system in each of two chambers

C.NO3 plantsBoth chambers contain KNO3(local and systemic signals indicate NO3 available)

C.KCl plantsBoth chambers contain KCl (local and systemic signals indicate NO3- deficiency)

Sp.NO3 roots experience locally high NO3- but also N-deficiency signals derived from Sp.KCl roots

Sp.KCl rootsExperience locally deficient NO3-conditions but also N-sufficient signals from Sp.NO3 roots

Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K.D. and Coruzzi, G.M. (2011). Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc. Natl. Acad. Sci. USA 108: 18524-18529.


Evidence for a systemic signal of N-demand on root development

Signals from the N-replete Sp.NO3 roots supress root growth in Sp.KCl as compared to C.KCl roots, indicating that a response to systemic N-repletion signals

Signals from the N-deficient roots promote elevated root growth in Sp.NO3 as compared to C.NO3, indicating that a response to systemic N-starvation signals

Model: Systemic signals promote root growth and suppress root growth

Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K.D. and Coruzzi, G.M. (2011). Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc. Natl. Acad. Sci. USA 108: 18524-18529. Li, Y., Krouk, G., Coruzzi, G.M. and Ruffel, S. (2014). Finding a nitrogen niche: a systems integration of local and systemic nitrogen signalling in plants. J. Exp. Bot. 65: 5601-5610 by permission of Oxford University Press.


Evidence for cytokinin-dependent and –independent signals

Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K.D. and Coruzzi, G.M. (2011). Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc. Natl. Acad. Sci. USA 108: 18524-18529.

A separate signal that promotes root growth in plants with total N deprivation (C.KCl) still operates in CK-deficient plants, as shown by increased growth in C.KCl as compared to Sp.KCl conditions

In cytokinin deficient plants, there is no systemic N-demand induced increase in root length

*

Growth augmentation correlating to N-starvation


Model of the effects of (some) local and systemic signals

Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K.D. and Coruzzi, G.M. (2011). Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc. Natl. Acad. Sci. USA 108: 18524-18529. Guan, P., Wang, R., Nacry, P., Breton, G., Kay, S.A., Pruneda-Paz, J.L., Davani, A., and Crawford, N.M. (2014). Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. Proc. Natl. Acad. Sci. USA 111: 15267-15272. Tabata, R., Sumida, K., Yoshii, T., Ohyama, K., Shinohara, H., and Matsubayashi,Y. (2014). Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346: 343-346.

Local NO3 effect

SystemicSystemic

Loss-of-function receptor mutants for root-derived peptides do not downregulate root growth when N is abundant

WT LOF

Other factors that contribute to local and systemic signals include auxin, amino acids,

transcription factors and root-derived peptides


Model for transceptor action: NO3-competes for auxin transport

Beeckman, T. and Friml, J. (2010). Nitrate contra auxin: Nutrient sensing by roots. Devel. Cell. 18: 877-878 with permission from Elsevier. See also Krouk, G., et al and Gojon, A. (2010). Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Devel. Cell. 18: 927-937; Mounier, E., et al and Nacry, P. (2014). Auxin-mediated nitrate signalling by NRT1.1 participates in the adaptive response of Arabidopsis root architecture to the spatial heterogeneity of nitrate availability. Plant Cell Environ. 37: 162-174; Forde, B.G. (2014). Nitrogen signalling pathways shaping root system architecture: an update. Curr. Opin. Plant Biol. 21: 30-36.

NPF6.3

NO3-Auxin NPF6.3

NO3-Auxin

When NO3- is low, NPF6.3 transports auxin away from the root tip and growth is inhibited

When NO3- is high, auxin transport through NPF6.3 is suppressed and growth is promoted


Strategies to improve nitrogen-use efficiency and decrease N pollution

Nolan, B.T. and Hitt, K.J. (2006). Vulnerability of shallow groundwater and drinking-water wells to nitrate in the United States. Environ. Sci. Technol. 40: 7834-7840. Image source: Lamiot; Alexandra Pugachevsky; NASA Earth Observatory

Nitrogen fixation is energy demanding

N ONNitrous oxide (N2O)

derived from fertilizer is a major greenhouse gas

Unhealthful nitrate from agricultural uses pollutes groundwater

Lake Erie

Cyanabacterial bloom


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Co-cropping and monitoring can decrease the need for N application

Apogee; N2Africa; Petr Kosina / CIMMYT. See also Muñoz-Huerta, R.F., Guevara-Gonzalez, R.G., Contreras-Medina, L.M., Torres-Pacheco, I., Prado-Olivarez, J., and Ocampo-Velazquez, R.V. (2013). A review of methods for sensing the nitrogen status in plants: Advantages, disadvantages and recent advances. Sensors. 13: 10823-10843; Robertson, G.P. and Vitousek, P.M. (2009). Nitrogen in agriculture: Balancing the cost of an essential resource. Annu. Rev. of Environ. Res. 34: 97-125.

Co-cropping or growing in rotation

with legumes enriches soil N content

Chlorophyll can be measured

the transmission

ratio of 653 nm to 931 nm light

N status can be determined by chlorophyll content, measured by reflected light


Slow-release fertilizers can match release to requirements

Adapted from Timilsena, Y.P., Adhikari, R., Casey, P., Muster, T., Gill, H. and Adhikari, B. (2014). Enhanced efficiency fertilisers: a review of formulation and nutrient release patterns. J. Sci. Food Agric. DOI: 10.1002/jsfa.6812

Traditional fertilizers don’t match nitrogen availability to plant needs. Slow release fertilizers can more closely match plant needs

Traditional fertilizer –one or two applications

Plant growth requirements

Slow-release fertilizer

Time

Am

ount

of f

ertil

izer

ava

ilabl

e

UREAN

N

NTime

Coated urea dissolves and releases slowly, but it can be expensive

H2OH2O


Soil bacteria can be manipulated to decrease N2O and NO3- pollution

Philippot, L. and Hallin, S. (2011). Towards food, feed and energy crops mitigating climate change. Trends Plant Sci. 16: 476-480 with permission from Elsevier. See also Subbarao, G.V., et al. 2009). Evidence for biological nitrification inhibition in Brachiaria pastures. Proc. Natl. Acad. Sci. USA. 106: 17302-17307. Subbarao, G.V., et al., (2013). A paradigm shift towards low-nitrifying production systems: the role of biological nitrification inhibition (BNI). Ann. Bot. 112: 297-316; Schipper, L.A., Robertson, W.D., Gold, A.J., Jaynes, D.B. and Cameron, S.C. (2010). Denitrifying bioreactors—An approach for reducing nitrate loads to receiving waters. Ecol. Engin. 36: 1532-1543.

Inhibitors of bacterial nitrification cause NH4+ to be retained in the soil, leading to less leaching and less N2O production

Denitrifying bacteria cultivated in a bioreactor downstream of a fertilized field protect waterways by converting NO3- in runoff to N2


Altering flux into amino acid pools can increase NUE

NH4+


(GS)

Glutamate



photorespiration


2-oxoglutarate

Glutamate



Assimilation

Remobilization

UptakePyruvate

AlanineAlanine

aminotransferase (AlaAT)

Storage

Good, A.G., Johnson, S.J., De Pauw, M., Carroll, R.T., Savidov, N., Vidmar, J., Lu, Z., Taylor, G. and Stroeher, V. (2007). Engineering nitrogen use efficiency with alanine aminotransferase. Can. J. Bot. 85: 252-262.


Breeding strategies for enhanced nitrogen use efficiency

Chardon, F., Noël, V. and Masclaux-Daubresse, C. (2012). Exploring NUE in crops and in Arabidopsis ideotypes to improve yield and seed quality. J. Exp. Bot. 63: 3401-3412 by permission of Oxford University Press; Martin, A., et al. and Hirel, B. (2006). Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell. 18: 3252-3274. Reprinted by permission from Macmillan Publishers Ltd: Sun, H., et al. (2014). Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet. 46: 652-656. Hirel, B., Le Gouis, J., Ney, B. and Gallais, A. (2007). The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J. Exp. Bot. 58: 2369-2387

Traits of an idealized plant with high NUE

Glutamine synthetaseactivity is an important component of NUE

In rice, a subunit of a heterotrimeric

G protein contributes to N-sensitive growth

and N assimilation


Summary: Improving N use efficiency in plants and soils

• N is abundant as N2, but often limiting for growth• N is fixed by biological or industrial means• N fertilization is economically and environmentally costly• N use efficiency involves uptake of NO3- and NH4+,

primary assimilation and recycling via GS / GOGAT• Regulatory and signaling pathways are being identified

as opportunities for breeding improvements• Monitoring of plant and soil N status can improve

fertilizer use efficiency


Phosphorus(note spelling – not phosphorous)

Reprinted from Blank, L.M. (2012). The cell and P: From cellular function to biotechnological application. Curr. Opin. Biotech. 23: 846 – 851 by permission of Elsevier.

• The 11th most abundant element in the earth’s crust

• The 5th most abundant element in a plant

• The 1st or 2nd most commonly limiting nutrient for plant growth

Phosphorus is one of the three major

macronutrients found in most fertilizers

P has roles in cell structure, energy and information storage and energy and information transfer


Phosphorus is an essential nutrient and found in many biomolecules

Membrane phospholipids

DNA and RNA

ATP

Phosphorus (P) is assimilated and used as phosphate (Pi) which depending on the pH is H2PO4- ,HPO42- or PO43-

HH H


Plants are part of the global phosphorus cycle: Preindustrial

Adapted from Smil, V. (2000). Phosphorus in the environment: Natural flows and human interference. Annu. Rev. Energy Environ. 25: 53–88 and Vaccari, D.A. (2000). Phosphorus: A looming crisis. Sci. Am. June: 54 – 59; Fixen, P.E. and Johnston, A.M. (2012). World fertilizer nutrient reserves: a view to the future. J. Sci. Food Agricul. 92: 1001-1005.

Essentially NO atmospheric pool of P

manuredecomposition

Terrestrial cycle: Plant / Animal / Soil

Slow leaching of P to lakes and oceans

Slow weathering of P from rock reserves to soil

Aquatic cycle

Sedimentation

Upwelling


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Plants are part of the global phosphorus cycle: Postindustrial

Adapted from Smil, V. (2000). Phosphorus in the environment: Natural flows and human interference. Annu. Rev. Energy Environ. 25: 53–88 and Vaccari, D.A. (2000). Phosphorus: A looming crisis. Sci. Am. June: 54 – 59. See also Elser, J. and Bennett, E. (2011). Phosphorus cycle: A broken biogeochemical cycle. Nature. 478: 29-31.

Essentially NO atmospheric pool of P

manuredecomposition


Mining and commercial processing accelerates P

entry to biosphere

Aquatic cycleModern practices accelerate runoff

Sewage

Urbanization removes P from terrestrial cycle and accelerates entry to waterways, causing toxic algal blooms (eutrophification)


Is the current rate of phosphorus use sustainable?

Adapted from Cordell, D., Drangert, J.-O. and White, S. (2009). The story of phosphorus: Global food security and food for thought. Global Environmental Change. 19: 292-305, and Great Quest.

United States

8%Morocco

38%

South Africa10%

Jordan6%

China27%

Manure

Phosphate rock

Human excretaGuano

1800 1900 20001950

Phosphate usage has increased dramatically in the past 70 years Some have argued that we

are approaching a period of “peak phosphorus” as deposits become depleted

90% of the world’s phosphate rock reserves are found in 5 countries


Phosphorus in soil is in the form of immobile, insoluble complexes

Lewis, D.G. and Quirk, J.P. (1967). Phosphate diffusion in soil and uptake by plants. Plant nd Soil. 26: 445-453; With kind permission from Springer Science and Business Media

Depletion Zone

Ca-P

Mg-PAl-PCation-phosphate complexes

are relatively insoluble and immobile in soil; these include oxides and hydroxides of Al and Fe

Organic phosphates

Fe-P

Plants don’t take up organic phosphate

Roots growing in 31P-labeled soil. Only P immediately next to roots is taken up


Plant and microbial exudates can increase Pi availability

Depletion Zone

Organic phosphates

Pi

Phosphatases (enzymes)

Pi

Low Molecular Weight Organic Acids (LMWOA)

Malate

Al-MalateAl-P

Exudates from free-living and symbiotic microbes also contribute to P solubilization

PhytateC6H18O24P6

Phytase-producing bacteria

Pi

Pi


Arbuscular mycorrhizal fungi facilitate P-uptake in most plants

Karandashov, V. and Bucher, M. (2005). Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci. 10: 22-29 with permission from Elsevier; see also Smith, S.E., Jakobsen, I., Grønlund, M. and Smith, F.A. (2011). Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 156: 1050-1057. (See also Teaching Tools in Plant Biology 19: Plants and their Microsymbionts).

~80% of plants associate with mycorrhizal fungi; these associations can facilitate P uptake


Root system architecture can optimize foraging for phosphate

Péret, B., Clément, M., Nussaume, L. and Desnos, T. Root developmental adaptation to phosphate starvation: better safe than sorry. (2011). Trends Plant Sci. 16: 442-450 with permission from Elsevier; Lynch, J.P. (2011). Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops. Plant Physiol. 156: 1041-1049.

Root traits associated with enhanced phosphate uptake:• Reduced gravitropism• Increased formation and elongation of

lateral roots and root hairs• Aerenchyma (air spaces that allow

metabolically inexpensive growth)

Aerenchyma


Lambers, H., Finnegan, P.M., Laliberté, E., Pearse, S.J., Ryan, M.H., Shane, M.W. and Veneklaas, E.J. (2011). Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: Are there lessons to be learned for future crops? Plant Physiol. 156: 1058-1066.

Many species of the family Proteaceae found throughout the Southern Hemisphere make short-lived “proteoid” or “cluster” roots to facilitate P uptake

Simple and compound Proteaceae root clusters

Banksia ericifolia flower


Cluster roots increase surface area and also root exudation

Cheng, L., Bucciarelli, B., Shen, J., Allan, D. and Vance, C.P. (2011). Update on white lupin cluster root acclimation to phosphorus deficiency Plant Physiol. 156: 1025-1032. Lambers, H., Clements, J.C. and Nelson, M.N. (2013). How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am. J. Bot.. 100: 263-288.

White lupin (Lupinus albus) is a cluster-root producing legume that provides a good genetic model


PHT1 phosphate transporters mediate uptake and transport

Nussaume, L., Kanno, S., Javot, H., Marin, E., Pochon, N., Ayadi, A., Nakanishi, T.M. and Thibaud, M.-C. (2011) Phosphate import in plants: focus on the PHT1 transporters. Front. Plant Sci. 2: 83. Pedersen, B.P., et al and and Stroud, R.M. (2013). Crystal structure of a eukaryotic phosphate transporter. Nature. 496: 533-536. Loth-Pereda, V.,et al. and Martin, F. (2011). Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal Populus trichocarpa. Plant Physiol. 156: 2141-2154. See also Lapis-Gaza, H.R., Jost, R., and Patrick M Finnegan, P.M. (2014). Arabidopsis PHOSPHATE TRANSPORTER1 genes PHT1;8 and PHT1;9 are involved in root-to-shoot translocation of orthophosphate. BMC Plant Biol. 14: 334.

Most are expressed in roots and other tissues

PHT transporters are H+/ PO43- co-transporters that have 12 membrane-spanning domains

9 PHT1 genes in Arabidopsis, 13 in rice, 12 in poplar. Some are mycorrhiza inducible


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P-Starvation Inducible responses increase P uptake and recycling

Huang, T.-K., et al and Lucas, W.J. (2014). Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J. Integr. Plant Biol. 56: 192-220 by permission. Sulpice, R., et al and Lambers, H. (2014). Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant Cell Environ. 37: 1276-1298. See also Lin, W.-Y., Huang, T.-K., Leong, S.J. and Chiou, T.-J. (2014). Long-distance call from phosphate: systemic regulation of phosphate starvation responses. J. Exp. Bot. 65: 1817-1827.

Proteaceae show metabolic adaptions to P-impoverished soils such as very efficient use of P

Ribosomes (rRNA) are the major form of organic P. Proteaceae maintain a very low copy number of ribosomes, yet are photosynthetically efficient

Proteaceae also show delayed greening; ribosomes first promote growth, then chloroplast maturation


PSI (phosphate-starvation induced) are upregulated by PHR1

Puga, M.I., Mateos, I., Charukesi, R., Wang, Z., Franco-Zorrilla, J.M., de Lorenzo, L., Irigoyen, M.L., Masiero, S., Bustos, R., Rodríguez, J., Leyva, A., Rubio, V., Sommer, H. and Paz-Ares, J. (2014). SPX1 is a phosphate-dependent inhibitor of PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis. Proc. Natl. Acad. Sci. USA 111: 14947-14952; Wang, Z., Ruan, W., Shi, J., Zhang, L., Xiang, D., Yang, C., Li, C., Wu, Z., Liu, Y., Yu, Y., Shou, H., Mo, X., Mao, C. and Wu, P. (2014). Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc. Natl. Acad. Sci. USA 111: 14953-14958.

PSI genes encode phosphatases, transporters, regulatory factors….

SPX1 interferes with PHR1 binding to its DNA binding site (P1BS). In yeast, SPX1 proteins act as Pi sensors

The interaction between SPX1 and PHR1 is Pi-dependent….


Regulatory controls prevent Pi from over accumulating

Delhaize, E., and Randall, P.J. (1995). Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol. 107: 207 – 213; Liu, T.-Y., Huang, T.-K., Tsenga, C.-Y., Lai, Y.-S., Lin, S.-I., Lin, W.-Y., Chen, J.-W., Chiou, T.J. (2012). PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 24: 2167 – 2183.

PHO1 is a transporter that moves Pi into xylem for transport to the shoot

PHT transporters take up Pi

PHO1

PHO2

PHO2 is an E2 ligase that targets

transporters for proteolysis

In pho1 mutants, too much Pi accumulates

in the root and too little in the shoot

In pho2 mutants, too much Pi

accumulates in the shoot and too little

in the root; transport is out-of-control

Too much or too little is badPi

Pi

xyle

m

root

shoot

PHTPHO1


Mutants pho1 and pho2 show effects of altered Pi transport

Liu, T.-Y., Lin, W.-Y., Huang, T.-K. and Chiou, T.-J. MicroRNA-mediated surveillance of phosphate transporters on the move. Trends Plant Sci. 19: 647-655 with permission from Elsevier.


PHO2 accumulation is regulated by miR399 expression

Redrawn from Franco-Zorrilla, J. M., Valli, A., Todesco, M., Mateos, I., Puga, M.I., Rubio-Somoza, I., Leyva, A., Weigel, D., García, J.A., and Paz-Ares, J. (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39: 1033–1037.

PHO2

PHO2 mRNA

+ Pi

PHO1

P starvation induces expression of miR399,

which targets PHO2 mRNA for degradation

PHO1

PHO2

PHO2 mRNA

- Pi

Pi

xyle

m

Pi

PHO2

miR399

miR399IPS1

A target mimic IPS1fine-tunes the effects of miR299; by binding stably to miR399, IPS1 supports PHO2 expression

When Pi is ample, PHO2 targets PHO1 for

degradation

PHO2


P uptake & transport are regulated by local and systemic signals

Wu, P., Shou, H., Xu, G. and Lian, X. (2013). Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr. Opin. Plant Biol. 16: 205-212. Liu, T.-Y., Lin, W.-Y., Huang, T.-K. and Chiou, T.-J. (2014). MicroRNA-mediated surveillance of phosphate transporters on the move. Trends Plant Sci. 19: 647-655.

Strigolactones

Phosphate starvation

signal (unknown) PHR1

(transcription factor)

PHT1 transporters

Phosphatases, organic acid synthases

miR399

Suppression of shoot branching

Establishment of plant – mycorrhizal

fungi symbiosis

Enhanced uptake

PHO2 PHT1

(miR399 is a negative regulator of a negative regulator of P uptake)IPS1

PHO1


Strategies to improve crop plant phosphorus use efficiency

Vinod, K.K. and Heuer, S. (2012). Approaches towards nitrogen- and phosphorus-efficient rice. AoB Plants. 2012: pls028


Many different transgenic lines have been tested for enhanced P uptake

Wu, P., Shou, H., Xu, G. and Lian, X. (2013). Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr. Opin. Plant Biol. 16: 205-212 with permission from Elsevier.

Modifying regulators of P signaling network

Releasing Pi from insoluble pools (through organic acid extrusion, proton pumping, and phosphatases)

Optimizing root architecture

Enhancing high affinity uptake (PHT1 transporter)

Success has been mixed


Selection for root architecture traits can lead to increased P uptake

Lynch, J.P. (2011). Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops. Plant Physiol. 156: 1041-1049; Wang, X., Yan, X. and Liao, H. (2010). Genetic improvement for phosphorus efficiency in soybean: a radical approach. Ann. Bot. 106: 215-222 by permission of Oxford University Press.

P-uptake efficiency can be correlated to more efficient root traits

P-efficient root system

P-inefficient root system

P-efficient root system P-inefficient root system


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Rice adapted to poor-soil regions revealed a key protein kinase

Reprinted by permission from Macmillan Publishers Ltd : Gamuyao, R., Chin, J.H., Pariasca-Tanaka, J., Pesaresi, P., Catausan, S., Dalid, C., Slamet-Loedin, I., Tecson-Mendoza, E.M., Wissuwa, M. and Heuer, S. (2012). The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature. 488: 535-539.See also Chin, J.H., Gamuyao, R., Dalid, C., Bustamam, M., Prasetiyono, J., Moeljopawiro, S., Wissuwa, M. and Heuer, S. (2011). Developing rice with high yield under phosphorus deficiency: Pup1 sequence to application. Plant Physiol. 156: 1202-1216.

• The Pup1 (Phosphate Uptake 1) major QTL was identified in aus-variety rice adapted to poor soils

• Eventually this was revealed to encode a protein kinase PSTOL1 not present in other rice genomes

• Overexpression of PSTOL1 leads to enhanced root growth

Overexpressor Control


Is it feasible to reuse, recapture and recycle phosphate?

Urine-reclaiming toilet

Phosphate recovered from human urine alone could replace >20% of phosphate demands

Human urine is rich in phosphate, and it can be separated from other waste at the point of origin

Urine can be applied directly to plants as liquid fertilizer

N & P-rich Wastewater in

PP

Mg

Mg

Struvite (NH₄MgPO₄·6H₂O) crystals harvested for use as fertilizer

Cleaner wastewater

out

P an

d N

can

be

prec

ipita

ted

out o

f was

tew

ater

Pratt, C., Parsons, S.A., Soares, A. and Martin, B.D. (2012). Biologically and chemically mediated adsorption and precipitation of phosphorus from wastewater. Curr. Opin. Biotechnol. 23: 890-896; Mihelcic, J.R., Fry, L.M. and Shaw, R. (2011). Global potential of phosphorus recovery from human urine and feces. Chemosphere. 84: 832-839.. Multiformharvest.com


Strategies have been developed to impede P from entering waterways

McDowell, R.W. (2012). Minimising phosphorus losses from the soil matrix. Curr. Opin. Biotech. 23: 860-865 with permission from Elsevier; Pratt, C., Parsons, S.A., Soares, A. and Martin, B.D. (2012). Biologically and chemically mediated adsorption and precipitation of phosphorus from wastewater. Curr. Opin. Biotech. 23: 890-896 Shilton, A.N., Powell, N. and Guieysse, B. (2012). Plant based phosphorus recovery from wastewater via algae and macrophytes. Curr. Opin. Biotech. 23: 884-889 by permission from Elsevier, and others from the same issue. Rittmann, B.E., Mayer, B., Westerhoff, P. and Edwards, M. (2011). Capturing the lost phosphorus. Chemosphere. 84: 846-853. Schipper, W. (2014). Phosphorus: Too big to fail. Eur. J. Inorgan. Chem. 2014: 1567-1571.

Timing of fertilizer application and management of water flow from can decrease

the amount of P that enters waterways

Chemical and biological processes including algal production can

effectively remove P from wastewaters


Summary: Phosphorus

• First or second most commonly limiting nutrient• Very insoluble and immobile in soil• Roots mine and forage for P through exudations and

symbioses• Root system architecture is particularly sensitive to P• Uptake involves positive and negative controls• Strategies are available to minimize P pollution


Potassium: Potash, from the ashes in the pot

Regulates stomatal

conductance, photosynthesis

and transpiration

Maintains turgor and reduces wilting

Strengthens cell walls

Maintains ionic balanceStimulates

photosynthate translocation

Enhances fertility

Promotes stress tolerance

See Wang, M., Zheng, Q., Shen, Q. and Guo, S. (2013). The critical role of potassium in plant stress response. Intl. J. Mol. Sci. 14: 7370-7390; Sin Chee Tham /Photo; Purdue extension; Onsemeliot.

Symptoms of potassium deficiency

[K+] in soil = ~0.1 – 1 mM[K+] in plant cell cytoplasm = ~100 mM

Potassium is an essential macronutrient

Regulates enzyme activities


Potassium fertilizers are mined from underground reserves as “potash”

Almost half of the world’s reserved of potash are found in Saskatchewan, Canada

Potash is a term that encompasses many forms of potassium:• KCl (potassium chloride, aka sylvite)• K2SO4 (potassium sulfate)• K2CO3 (potassium carbonate)• K2Ca2Mg(SO4)4·2H2O (polyhalite)• etc.

Canada Potash; Lmbuga

KCl, sylvite

For historical reasons, potash is measured in units of K2O equivalents, even though it is rarely found in the form of K2O


Potash provides K for fertilizers, which supplement natural sources

manuredecomposition


Underground reserves

Water with dissolved K+

salts returned to surface

Water pumped

underground

Salts recovered by evaporation

90 – 98% insoluble minerals

1 – 3% exchangeable

salts

0.1 – 0.2% soil solution K+

Potash fertilizer

application

Adapted from International Potash Institute


Potash prices can be volatile and there are few suppliers

1.06 cm

Canada is #1 in production (11.2 Mt) and

reserves (4,400 Mt)

Russia is #2 in production (7.4 Mt) and

reserves (3,300 Mt)

Brazil3.2 Mt210 Mt

Chile0.8 Mt130 Mt

US1.1 Mt130 Mt

China3.2 Mt210 Mt

Belarus5.5 Mt750 Mt

World reserves9500 Mt

World production

(2011) 37 Mt

Jordan1.4 Mt40 Mt

Israel2.0 Mt40 Mt

Germany3.3 Mt150 Mt

Spain0.4 Mt20 Mt

UK0.4 Mt22 Mt

Adapted from International Potash Institute


Potassium is an essential plant nutrient

Reprinted from Maathuis, F.J.M. (2009). Physiological functions of mineral macronutrients. Curr. Opin. Plant Biol. 12: 250-258 with permission from Elsevier.

K+ uptake involves high and low affinity transporters

K+ is a counter ion for negatively charged molecules including DNA and proteins

K+ is a cofactor for some enzymes

As the major cation in the vacuole, K+contributes to cell expansion and movement, including that of guard cells

K+ moves in and out of the vacuole through specific transporters


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Early studies of potassium uptake in plants: Biphasic uptake

Epstein, E., Rains, D.W., and Elzam, O.E. (1963). Resolution of dual mechanisms of potassium absorption by barley roots. Proc. Natl. Acad. Sci. USA. 49: 684 – 692; Gierth, M. and Mäser, P. (2007). Potassium transporters in plants – Involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett. 581: 2348-2356.

KCl (mM)

Low affinity transport

High affinity transport

Epstein et al showed two phases of K+uptake in barley roots

K+K+ H+

H+

ATP

2 x H+

2 x ATP

Low affinity transport

High affinity transport

K+ uptake from low [K+]extrequires more energy than when [K+]ext is higher

Co-transporter mediated

Channel mediated


K+ mobilization is critical for K+ use efficiency

Adapted from Amtmann, A., and Leigh, R. (2010). Ion homeostasis. In Abiotic Stress Adaptation in Plants: Physiological, Molecular and Genomic Foundation, A. Pareek, S.K. Sopory, H.J. Bohnert and Govindjee (eds) (Dordrecht, The Netherlands: Springer), pp. 245 – 262.

Cytosol

Vac.

Supraoptimal K+can be stored in the vacuole

As K+ becomes limiting, it becomes preferentially allocated to the cytosol


K+ mobilization is critical for K+ use efficiency

Cytosol

Vac.

Prioritized

Non-Prioritized

As K+ becomes limiting, it becomes preferentially allocated to the cytosol

K+ can be remobilized from less essential tissues into prioritized tissues such as growing and photosynthetic tissues

Adapted from Amtmann, A., and Leigh, R. (2010). Ion homeostasis. In Abiotic Stress Adaptation in Plants: Physiological, Molecular and Genomic Foundation, A. Pareek, S.K. Sopory, H.J. Bohnert and Govindjee (eds) (Dordrecht, The Netherlands: Springer), pp. 245 – 262.


Summary: Potassium uptake, transport and regulation

• Potassium is an essential macronutrient required in large amounts

• Potassium uptake involves low and high affinity transporters

• K+ uptake, transport and remobilization are regulated extensively to ensure that the plant’s critical tissues are preferentially supported


Sulfur: Clean air can lead to deficient plants

International Society of Arboriculture; Robert L. Anderson, USDA Forest Service; D'Hooghe, P., Escamez, S., Trouverie, J. and Avice, J.-C. (2013). Sulphur limitation provokes physiological and leaf proteome changes in oilseed rape that lead to perturbation of sulphur, carbon and oxidative metabolisms. BMC Plant Biol. 13: 23. Hay and Forage.

Sulfur dioxide damage

Until recently, sulfur dioxide emission from fossil fuel combustion led to acid rain and extensive damage to vulnerable plants

Eliminating S from air pollution uncovered crop plant deficiencies, particularly in oilseed rape and wheat


Sulfur can be found in many inorganic forms

Species Name Oxidation State

S2‐, H2S, R‐SH Sulfide ‐2S0, S8 Sulfur 0SO2 Sulfur dioxide (toxic gas) +4SO3‐ Sulfite +4SO42‐ Sulfate +6

Plants take up sulfur from soil as SO42- and to a lesser extent from the atmosphere as SO2 or H2S

Organic SR-SH

SO42-

S0

H2S

Sulfur deposits

SO3-


Plants are an important part of the global sulfur cycle

Atmospheric pool of sulfur – mostly SO2 (sulfur dioxide)Combustion of fossil fuels

Prokaryotic oxidation

R-SH

manureAssimilation

by plantsdecomposition

SO2 SO42-H2OO2

SO42-S

Volcanic activity

SO42-

Acid rain*

*Since the 1980s, SO2 emissions and SO42- precipitation have been declining

H2S

Prokaryotic reduction

See for example Takahashi, H., Kopriva, S., Giordano, M., Saito, K. and Hell, R. (2011). Sulfur assimilation in photosynthetic organisms: Molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62: 157-184.


Sulfur is an essential macronutrient in amino acids & other compounds

HS-CH2-CH-COOHNH2

H3C-S-CH2-CH2-CH-COOHNH2

Methionine (Met)

Cysteine (Cys)

Amino acids

CysGlutathioneGlutathione is an amino acid derivative involved in Redox reactions

Oxidation /reduction, metal transport and detox

S

Allicin (garlic flavor)

Allyl-isothiocyanate (horseradish flavor)

Flavor or odor

SHO

Mercapto-p-menthan-3-one (blackcurrant)

S S

S S

DefenseGlucosinolates are anti-herbivores

Camalexin is a defense compound induced by pathogens

S

S

McGorrin, R.J. (2011). The significance of volatile sulfur compounds in food flavors. Volatile Sulfur Compounds in Food. ACS Symposium Series, Vol. 1068: 3-31


Sulfate uptake occurs primarily through SULTR transporters

Buchner, P., Takahashi, H. and Hawkesford, M.J. (2004). Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J. Exp. Bot. 55: 1765-1773 with permission from Oxford University Press; Smith, F.W., Ealing, P.M., Hawkesford, M.J. and Clarkson, D.T. (1995). Plant members of a family of sulfate transporters reveal functional subtypes. Proc. Natl. Acad. Sci. USA 92: 9373-9377. Rouached, H., Secco, D. and Arpat, A.B. (2009). Getting the most sulfate from soil: Regulation of sulfate uptake transporters in Arabidopsis. J. Plant Physiol. 166: 893-902. Gojon, A., Nacry, P. and Davidian, J.-C. (2009). Root uptake regulation: a central process for NPS homeostasis in plants. Curr. Opin. Plant Biol. 12: 328-338.

In Arabidopsis, 12 genes encode SULTR transporters that

fall into four groups

Most are 12-membrane spanning SO42- / H+ co-transporters

SO42- H+

SO42- H+

Primary assimilation in roots occurs mainly through SULTR1;1 and SULTR1;2


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In higher plants, SULTR transporters effect inter-organelle movement

Buchner, P., Takahashi, H. and Hawkesford, M.J. (2004). Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J. Exp. Bot. 55: 1765-1773; Gigolashvili, T. and Kopriva, S. (2014). Transporters in plant sulfur metabolism. Frontiers in Plant Science. 5: 442. Rennenberg, H. and Herschbach, C. (2014). A detailed view on sulphur metabolism at the cellular and whole-plant level illustrates challenges in metabolite flux analyses. J. Exp. Bot. 65 : 5711-5724.

Vacuole

Plastid

Cytosol

[SO42-] 6 – 75 mM

[SO42-] ≤ 10 μM

[SO42-] 1 – 11 mM

[SO42-] 4 – 12 mM

SO42- H+

SULTR

SO42-

H+

SULTR

SO42-

H+

STORAGE

SULTR

SO42-

S2-

Sulfate reduction only

occurs in plastids


Buchner, P., Takahashi, H. and Hawkesford, M.J. (2004). Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J. Exp. Bot. 55: 1765-1773 by permission of Oxford University Press.

S transporters coordinate long-distance transport too


Hell, R. and Markus Wirtz, M. (2011). Molecular Biology, Biochemistry and Cellular Physiology of Cysteine Metabolism in Arabidopsis thaliana. The Arabidopsis Book 9: e0154.

Uptake

Adenosine 5'-phosphosulfate

5'-Phosphoadenosine 3'-phosphosulfate

Primary sulfur metabolism (overview)


Sulfate is assimilated by ATP sulfurylase into APS

Sulfate ATP

+

Pyrophosphate (PPi) Adenosine 5'-

phosphosulfate (APS)

+

ATP sulfurylase

Adapted from Takahashi, H., Kopriva, S., Giordano, M., Saito, K. and Hell, R. (2011). Sulfur assimilation in photosynthetic organisms: Molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62: 157-184.

This reaction occurs in the cytosol and plastid


APS can enter two pathways for primary or secondary reactions

Adenosine 5'-phosphosulfate (APS)

APS kinase

ATP

ADP

5'-Phosphoadenosine 3'-phosphosulfate (PAPS)

Sulfated compounds, glucosinolates

APS reductase

Sulfite reductaseSulfite Sulfide

AMP

SO32- S2-2 GSH

GSSGFdxRed

FdxOx

Cysteine

Located exclusively in plastids

Adapted from Takahashi, H., Kopriva, S., Giordano, M., Saito, K. and Hell, R. (2011). Sulfur assimilation in photosynthetic organisms: Molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62: 157-184.


Sulfide is assimilated into cysteine by the cysteine synthase complex

Reprinted from Jez, J.M. and Dey, S. (2013). The cysteine regulatory complex from plants and microbes: what was old is new again. Curr. Opin. Structural Biol. 23: 302-310 with permission from Elsevier.

O-acetylserine (OAS) indicates cellular S status: when S is low, OAS accumulates

Adenosine 5'-phosphosulfate (APS)

(thiol)lyase (OAS-TL)

Cysteine synthase is a complex of SAT and OAS-TL, and is present in the cytosol, plastid and mitochondria


Model for regulation of cysteine synthesis by the CS complex

Reprinted from Jez, J.M. and Dey, S. (2013). The cysteine regulatory complex from plants and microbes: what was old is new again. Curr. Opin. Structural Biol. 23: 302-310 with permission from Elsevier.Hell, R. and Markus Wirtz, M. (2011). Molecular Biology, Biochemistry and Cellular Physiology of Cysteine Metabolism in Arabidopsis thaliana. The Arabidopsis Book 9: e0154.

When SO42- is available, free OAS-TL dimers produce cysteine

OAS is synthesized by SAT within the cysteine synthase (CS) complex

SATCSOAS-TL is inactive within the CS complex


Model for regulation of cysteine synthesis by the CS complex

Hell, R. and Markus Wirtz, M. (2011). Molecular Biology, Biochemistry and Cellular Physiology of Cysteine Metabolism in Arabidopsis thaliana. The Arabidopsis Book 9: e0154.

When SO42- is unavailable, OAS accumulates, causing the CS complex to dissociate, and decreasing the activity of SAT. Thus, the rate of production of OAS decreases

Free SAT is deactivated


Sulfur uptake and assimilation rates are metabolically regulated

Adapted from Takahashi, H., Kopriva, S., Giordano, M., Saito, K. and Hell, R. (2011). Sulfur assimilation in photosynthetic organisms: Molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62: 157-184; Davidian, J.-C. and Kopriva, S. (2010). Regulation of sulfate uptake and assimilation—the same or not the same? Mol. Plant. 3: 314-325. Yi, H., Galant, A., Ravilious, G.E., Preuss, M.L. and Jez, J.M. (2010). Sensing sulfur conditions: Simple to complex protein regulatory mechanisms in plant thiol metabolism. Mol. Plant. 3: 269-279.

SO42-out

SO42-in

SULTR

APS Reductase

Cys SynthaseSO3-

Cys

Transcriptional, post-transcriptional and post-translational / allosteric regulation of transporters

Local sulfate levels

OAS

OAS

Allosteric interactions, metabolic regulation

Reduced sulfur (glutathione, Cys etc)

Light, carbon and nitrogen reserves,

circadian rhythms etc)

Transcriptional regulation of ATP sulfurylase and adenosine 5'-phosphosulfate (APS) reductase (APR)

ATP Sulfurylase


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SLIM (EIL3) coordinates many transcriptional responses to S

Maruyama-Nakashita, A., Nakamura, Y., Tohge, T., Saito, K. and Takahashi, H. (2006). Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell. 18: 3235-3251.

SLIM = Sulfur LimitationRed, pink = up-regulated by S-deficiencyBlue = down-regulated by S-deficiency

Thioglucosidase activity (increased by S-deficiency) liberates S for recycling


Addressing S deficiency in plants

D'Hooghe, P., Escamez, S., Trouverie, J. and Avice, J.-C. (2013). Sulphur limitation provokes physiological and leaf proteome changes in oilseed rape that lead to perturbation of sulphur, carbon and oxidative metabolisms. BMC Plant Biol. 13: 23. Hay and Forage.

S sufficient S deficientWith stricter laws on S emissions, less S enters soils and plants are more prone to S deficiency

Soil can be augmented with elemental sulfur, ammonium sulfate or other fertilizers


Summary: Sulfur uptake and metabolism

• Found in many redox forms and can be assimilated from atmosphere

• Deficiency more common with cleaner air• SULTR transporter family primarily involved in uptake

and transport• Uptake and assimilation into organic forms subject to

positive and negative regulation


Magnesium: The “forgotten element”

Didier Descouens; Ra’ike; chensiyuan; James St. John

Mg in solution is a divalent cation Mg2+

Soil magnesium is a result of rock weathering and Mg2+from seawater

Serpentine3MgO*2SiO2*2H2O

The Dolomite Mountains are named for the mineral dolomiteMgCO3*CaCO3

Magnesite MgCO3


Magnesium is a cofactor for many enzymes and central to chlorophyll

Mg2+ is a counter ion for the negative charges of ATP

Mg2+stabilizes ribosome 3D structure

Mg2+ is central to chlorophyll

Mg2+ is an essential activator for many enzymes including Rubisco

Jensen, R.G. (2000). Activation of Rubisco regulates photosynthesis at high temperature and CO2. Proc. Natl. Acad. Sci. USA 97: 12937-12938.


Mg deficiency interferes with photosynthesis & C transport

Reused with permission from Wiley from Cakmak, I. and Kirkby, E.A. (2008). Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol. Plant. 133: 692-704; See also Verbruggen, N., and Hermans, C. (2013). Physiological and molecular responses to magnesium nutritional imbalance in plants. Plant Soil. 368: 87 – 99.

Effects of Mg deficiency

One symptom of Mg deficiency is high-light induced chlorosis


Magnesium transporters move Mg2+ across membranes

Reproduced from Hermans, C., Conn, S.J., Chen, J., Xiao, Q. and Verbruggen, N. (2013). An update on magnesium homeostasis mechanisms in plants. Metallomics. 5: 1170-1183 with permission of The Royal Society of Chemistry; Reprinted by permission from Macmillan Publishers Ltd Hattori, M., Tanaka, Y., Fukai, S., Ishitani, R. and Nureki, O. (2007). Crystal structure of the MgtE Mg2+ transporter. Nature. 448: 1072-1075.

There are two known classes of Mg transporters:MRS/MGTMHX (Mg/H+ exchanger)

Proposed structure and mechanism of an MRS-type

transporter

Mg transporters are different from other cation transporters but conserved

across life domains


Magnesium uptake is mediated by the MRS / MGT family

Gebert, M., Meschenmoser, K., Svidová, S., Weghuber, J., Schweyen, R., Eifler, K., Lenz, H., Weyand, K. and Knoop, V. (2009). A root-expressed magnesium transporter of the MRS2/MGT gene family in Arabidopsis thaliana allows for growth in low-Mg2+ environments. Plant Cell. 21: 4018-4030. Mao, D., Chen, J., Tian, L., Liu, Z., Yang, L., Tang, R., Li, J., Lu, C., Yang, Y., Shi, J., Chen, L., Li, D. and Luan, S. (2014). Arabidopsis transporter MGT6 mediates magnesium uptake and is required for growth under magnesium limitation. Plant Cell. 26: 2234-2248.

MGT6 RNAi WT

MGT6 is induced in roots by low Mg and required for efficient Mg uptake


Aluminum toxicity is minimized by increased Mg uptake

Delhaize, E., and Ryan, P.R. (1995). Aluminum toxicity and tolerance in plants. Plant Physiol. 107: 315 – 321. Bose, J., Babourina, O. and Rengel, Z. (2011). Role of magnesium in alleviation of aluminium toxicity in plants. J. Exp. Bot. 62: 2251-2264, by permission of Oxford University Press.

Al tolerant

Al sensitive

Al inhibits growth, especially in low pH soils where it is most soluble

Elevated Mg soil levels or uptake can minimize Al toxicity mainly through competition for uptake and molecular interactions


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Mg deficiency in plants contributes to Mg deficiency in animals

Peggy Greb USDA

Rapidly growing spring grass can be low in Mg, so grass-fed cattle can experience hypomagnesemia, a sometimes fatal condition called grass tetany

Mg2+

To ensure adequate dietary Mg2+, human diets should include nuts, legumes, leaves and whole grains


Summary: Magnesium

• Rarely limiting for plant growth• Mg2+ transporters are different from other cation

transporters, but conserved across life domains• Elevated Mg2+ uptake can mitigate Al3+ toxicity • Humans and animals can suffer Mg deficiency if dietary

sources are deficient


Calcium: Low free cytosolic levels & functions in apoplast / vacuole

Capoen, W., Den Herder, J., Sun, J., Verplancke, C., De Keyser, A., De Rycke, R., Goormachtig, S., Oldroyd, G. and Holsters, M. (2009). Calcium spiking patterns and the role of the calcium/calmodulin-dependent kinase CCaMK in lateral root base nodulation of Sesbania rostrata. Plant Cell. 21: 1526-1540. Bose, J., Pottosin, I., Shabala, S.S., Palmgren, M.G. and Shabala, S. (2011). Calcium efflux systems in stress signalling andadaptation in plants. Front. Plant Sci. 2: 85. Persson, S., Caffall, K.H., Freshour, G., Hilley, M.T., Bauer, S., Poindexter, P., Hahn, M.G., Mohnen, D. and Somerville, C. (2007). The Arabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. Plant Cell. 19: 237-255.

Middle lamella

Primary wallSecondary

wall

2 μm

Calcium stabilizes pectin in middle lamella

of cell walls

Cytosolic Ca2+ oscillations are second messengers in diverse responses


90% of the plant’s calcium can be in the form of calcium oxalate crystals

Webb, M.A. (1999). Cell-mediated crystallization of calcium oxalate in plants. Plant Cell. 11: 751-761; Franceschi, V.R. and Nakata, P.A. (2005). Calcium oxalate in plants: Formation and Function. Annu. Rev. Plant Biol. 56: 41-71. Kostman, T.A., Tarlyn, N.M., Loewus, F.A. and Franceschi, V.R. (2001). Biosynthesis of l-ascorbic acid and conversion of carbons 1 and 2 of l-ascorbic acid to oxalic acid occurs within individual calcium oxalate crystal idioblasts. Plant Physiol. 125: 634-640.

Idioblasts are specialized cells that form calcium

oxalate crystals and are illuminated by polarized light

(RI = raphide idioblastDI = druse idioplast)

• The crystals are formed by specialized cells called idioblasts

• Calcium oxalate crystals can function in defense

• Calcium oxalate crystals also can sequester excess calcium

Prismatic crystals from bean seed coat

Druse crystals from velvet leaf (Abutilon theophrasti)

Bundle of raphide crystals from grape leaf


Plants maintain very low levels of free cytosolic Ca2+

Stael, S., Wurzinger, B., Mair, A., Mehlmer, N., Vothknecht, U.C. and Teige, M. (2012). Plant organellar calcium signalling: an emerging field. J. Exp. Bot. 63: 1525-1542 by permission of Oxford University Press .

The concentration of free Ca2+ is ~ 10,000 fold lower in the cytosol than the apoplast

The challenge at the plasma membrane is to maintain low free internal Ca2+ (in contrast to the situation for most other nutrients)


Ca2+ transport systems include channels, pumps and antiporters

Kudla, J., Batistič, O. and Hashimoto, K. (2010). Calcium signals: The lead currency of plant information processing. Plant Cell. 22: 541-563.


Calcium deficiency causes cell wall defects and sometimes cell death

White, P.J. and Broadley, M.R. (2003). Calcium in plants. Ann. Bot. 92: 487-511. Maine.gov; David B. Langston, University of Georgia; University of Georgia Plant Pathology Archive Bugwood.org

Ca2+

Calcium is translocated in the xylem (apoplast) but not the phloem (symplast), meaning that it cannot be remobilized when external supplies are limited

Ca2+ deficiency in growing tissues causes weakness and death, leading to blossom end rot (left), tip burn (right) and bitter pit (bottom). Ca2+ deficiency also can result from a low rate of transpiration.


Calcium contributes to pectin crosslinking and stabilization

Sundar Raj AA, Rubila S, Jayabalan R, Ranganathan TV (2012) A review on pectin: Chemistry due to general properties of pectin and its pharmaceutical uses. 1:550 doi:10.4172/scientificreports.550 (adapted from Axelos and Thibault, 1991). Hepler, P.K. and Winship, L.J. (2010). Calcium at the cell wall-cytoplast interface. J. Integr. Plant Biol. 52: 147-160, with permission from Wiley.

Pectin is found in the middle lamella and the cell wall of a growing pollen tube

Middle lamella

Pectin is a galacturonic acid polymer. Calcium stabilizes the pectin and causes it to “gel”

Ca2+ interacting with pectin at tip of pollen tube

Molecular gastronomists react calcium with pectin-like polymers

to produce interesting foods

Ca2+

Pectin


Calcium oscillations are mediated by ion channels, pumps and carriers

Venkateshwaran, M., Cosme, A., Han, L., Banba, M., Satyshur, K.A., Schleiff, E., Parniske, M., Imaizumi-Anraku, H. and Ané, J.-M. (2012). The recent evolution of a symbiotic ion channel in the legume family altered ion conductance and improved functionality in calcium signaling. Plant Cell. 24: 2528-2545. Evans, N.H. and Hetherington, A.M. (2001). Plant physiology: The ups and downs of guard cell signalling. Curr. Biol. 11: R92-R94 with permission from Elsevier; Kudla, J., Batistič, O. and Hashimoto, K. (2010). Calcium signals: The lead currency of plant information processing. Plant Cell. 22: 541-563.

A model of the ionic fluxes that result in calcium oscillations around the nucleus during symbiotic interactions

Ca2+ oscillations contribute to guard cell functions

How Ca2+oscillations are decoded remains incompletely resolved


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Summary: Calcium

• Much of a plant’s calcium may be in the form of calcium oxalate crystals

• Free Ca2+ ion is mainly stored outside cytosol, in apoplast and vacuole

• Calcium has a structural role in cell walls, particularly pectin gelling

• Calcium has a signaling role conferred by transient spikes in cytosol


Macronutrients: Summary

• Macronutrients (N, P, K, S, Mg, Ca) are essential elements that must be acquired from the environment

• Soil microbes affect nutrient availability and uptake• Nutrient-specific transporters control uptake,

translocation and remobilization of mineral nutrients• Some macronutrients are assimilated into organic

compounds• Uptake and assimilation reactions are coordinated by

nutrient availability and demand• Replenishment of soil nutrients is essential for high-

yielding agricultural systems


Macronutrients - Summary

Diaz, R.J. and Rosenberg, R. (2008). Spreading Dead Zones and Consequences for Marine Ecosystems. Science. 321: 926-929.

The ecological impacts of agriculture are huge and growing – most of these hypoxic regions arose since 1950 and are attributed to human activities


Gerland, P., Raftery, A.E., Ševčíková, H., Li, N., Gu, D., Spoorenberg, T., Alkema, L., Fosdick, B.K., Chunn, J., Lalic, N., Bay, G., Buettner, T., Heilig, G.K. and Wilmoth, J. (2014). World population stabilization unlikely this century. Science. 346: 234-237.

Macronutrients - Summary

9.6 billion(2050)

7.2 billion (2012)

10.9 billion(2100)

WORLD POPULATION PROJECTIONDemand for food will not slow down during this century

We must find innovative solutions to the challenge of feeding the plants that feed us


Ongoing research: Learn how plants integrate different nutrient needs

Kellermeier, F., Armengaud, P., Seditas, T.J., Danku, J., Salt, D.E. and Amtmann, A. (2014). Analysis of the root system architecture of Arabidopsis provides a quantitative readout of crosstalk between nutritional signals. Plant Cell. 26: 1480-1496. White, P.J., George, T.S., Dupuy, L.X., Karley, A.J., Valentine, T.A., Wiesel, L. and Wishart, J. (2013). Root traits for infertile soils. Front. Plant Sci. 4: 19.

How do roots optimize growth when two or more nutrients are limiting?

Cluster analysis of root traits that enhance

acquisition of various nutrients

Interactive effects of nutrients and daylength on root growth

How can understanding this integration support breeding efforts?


Ongoing research: Use best practices for nutrient management

International Plant Nutrition Institute; See also American Society of Agronomy; Video link Plant Nutrition Institute

Manage nutrients properly, using

the “4Rs”

Right Right

RightRight

NH4NO3 or Urea?

How much?

Between rows? On surface or deep?

Before planting? During vegetative

growth phase?

Continue to develop technologies to ensure optimal fertilizer use,

and make them affordable

Documents

The Plant Cell, December 2014 © 2014 12/12/2014 The American …€¦ · 20/01/2015 · • Plants get the rest of their nutrients as mineral nutrients • Mineral nutrients are