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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)
© 2014 American Society of Plant Biologists
“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
© 2014 American Society of Plant Biologists
“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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
The Plant Cell, December 2014 © 2014The American Society of Plant Biologists
12/12/2014
www.plantcell.org/cgi/doi/10.1105/tpc.114.tt1214 2
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
Soil pH affects nutrient availability-Some soils are acidic, others basic
Atlas of the biosphere, University of Wisconsin; FMoeckel
Strongly acidic
Mildly alkaline
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
Global mineral nutrient resources are unevenly distributed
Supply > Demand
Supply < Demand
FAO (2011) Current world fertilizer trends and outlook to 2015.
NP2O5K2O
© 2014 American Society of Plant Biologists
The global trade in fertilizers is worth billions of dollars annually
IFIA
Ammonium Urea Potash Diammonium phosphate
Monoammonium phosphate
Phosphate rock
Sulfur Sulfuric acid
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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?
© 2014 American Society of Plant Biologists
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.
The Plant Cell, December 2014 © 2014The American Society of Plant Biologists
12/12/2014
www.plantcell.org/cgi/doi/10.1105/tpc.114.tt1214 3
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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?
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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….
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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)
The Plant Cell, December 2014 © 2014The American Society of Plant Biologists
12/12/2014
www.plantcell.org/cgi/doi/10.1105/tpc.114.tt1214 4
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
Primary N assimilation: NO3- is reduced to NH4+ prior to assimilation
Uptake
NO3-
NH4+
NH4+
NO3-
Nitrate reductase
NO2-
Nitrite reductase
Glutamine synthetase
(GS)
Glutamine
Assimilation into organic compounds
All other N-containing compounds
R-NH3
Glutamate
© 2014 American Society of Plant Biologists
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-
© 2014 American Society of Plant Biologists
GS/GOGAT assimilates inorganic nitrogen into organic molecules
NH4+
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)
Assimilation
Remobilization
Uptake
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
Summary: Plant nitrogen uptake and assimilation
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.
© 2014 American Society of Plant Biologists
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)
The Plant Cell, December 2014 © 2014The American Society of Plant Biologists
12/12/2014
www.plantcell.org/cgi/doi/10.1105/tpc.114.tt1214 5
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
Altering flux into amino acid pools can increase NUE
NH4+
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)
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
Terrestrial cycle: Plant / Animal / Soil
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)
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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….
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
Potash provides K for fertilizers, which supplement natural sources
manuredecomposition
Terrestrial cycle: Plant / Animal / Soil
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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-
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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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© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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)
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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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© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
The Plant Cell, December 2014 © 2014The American Society of Plant Biologists
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© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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)
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
The Plant Cell, December 2014 © 2014The American Society of Plant Biologists
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© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
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?
© 2014 American Society of Plant Biologists
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
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