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

1. Plant Nutrition 2: Macronutrients (N, P, K, S, Mg and Ca) • Plants assimilate mineral nutrients from their surroundings • Nutrient assimilation can occur across the surface of the plant or through the root system of vascular plants PO43- PO43- PO43- PO43- PO43- PO43- K+ K+ K+ K+ K+ K+ K+ K+ NO3- NO3- NO3- NO3-

2. Plants assimilate mineral nutrients mainly as cations or anions 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

3. Nutrient uptake, assimilation and utilization involve many processes Nutrient uptake efficiency Nutrient utilization efficiency Root exudates Root system architecture Assimilation and remobilization efficiency NH3 Intercellular transport efficiency N N Transporters and pumps Regulatory networks Symbioses R-X X Rhizosphere microbiota P P

4. Physical and biological processes affect nutrient availability Erosion, rainfall patterns, cultural practices, soil biodiversity, soil pH, atmospheric gases etc. all affect soil fertility Plant-controlled Optimal pH range 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.

5. Nutrients removed from soils can be replenished with fertilizers Total nutrient requirement 1000 Plants remove nutrients from the soil Fertilizers can be complex waste products or refined blends of nutrient salts 800 Cotton Wheat Rice 600 Sulfur Corn Soy Magnesium Kg/ha 400 Potash 200 Phosphate Nitrogen Most fertilizers contain nitrogen (N), phosphorus (P) and potassium (K). Some include other elements 0 Typical fertilizer application 400 200 Kg/ha 0 Source: USGS

6. How much is the right amount of fertilizer to apply to a field? Cultivation practices: Is unharvested material removed, or left to replenish the soil? Species / variety of plant: Different plants have different needs Abiotic and biotic factors: Temperature, rain, stress and pests or pathogens affect nutrient needs Soil characteristics: Residual nutrients, rate of nutrient leaching, pH, particle size, presence of microbes etc. affect optimal application 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 Photo by Michael Russelle.

7. Fertilizer use can cause environmental and health problems Nitrogen fixation is energy demanding Human and animal waste can spread disease N N O Nitrous oxide (N2O) derived from fertilizer is a major greenhouse gas Transport requires energy Plants need nutrients, but their application isn’t always optimal or sustainable – how can plant science contribute to better practices? Phosphate and potash mining is destructive Nutrient runoff pollutes waterways and can lead to eutrophication Image source: Lamiot; Alexandra Pugachevsky

8. 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 N is in amino acids (proteins), nucleic acids (DNA, RNA), chlorophyll, and countless small molecules Nitrogen is one of the three major macronutrients found in most fertilizers 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.

9. Plants are an important part of the global nitrogen cycle Atmospheric pool of N2 Atmospheric fixation Industrial fixation Biological fixation 5 Tg N / yr Biological fixation (oceans) NO3- manure decomposition NH4+ NO3- R-NH2 NO3- Denitrification by denitrifying bacteria Assimilation by plants NH4+ 140 Tg N / yr 120 Tg N / yr 120 Tg N / yr (50% agricultural) NH4+ NO2- NO3- Nitrification by nitrifying bacteria Adapted from Fowler, D., et al. (2013). The global nitrogen cycle in the twenty-first century. Phil. Trans. Roy. Soc. B: 368: 20130164

10. Nitrogen metabolism: Uptake, assimilation and remobilization Carbon pools TCA cycle Amino acid recycling, photorespiration Remobilization Uptake Glutamate Assimilation 2-oxoglutarate NH4+ Glutamine-2-oxoglutarate aminotransferase (GOGAT) NH4+ Nitrite reductase NO2- Glutamate Nitrate reductase Glutamine synthetase (GS) Glutamine Incorporation into amino acids and other nitrogen-containing compounds NO3- NO3- R-NH2 NH4+ Assimilation 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.

11. Roots respond to local and systemic nitrogen availability When nitrogen is abundant, plants allocate less biomass to their roots When nitrogen distributionis patchy, roots proliferate in the nutrient rich patches 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.

12. Phosphorus(note spelling – not phosphorous) • The 11th most abundant element in the earth’s crust • The 5th most abundant element in a plant • The 2nd most commonly limiting nutrient for plant growth P has roles in cell structure, energy and information storage and energy and information transfer Phosphorus is one of the three major macronutrients found in most fertilizers 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.

13. Phosphorus is an essential nutrient and found in many biomolecules Membrane phospholipids DNA and RNA Phosphorus (P) is assimilated and used as phosphate (Pi) which depending on the pH is H2PO4- ,HPO42- or PO43- ATP H H H

14. Phosphorus in soil is in the form of immobile, insoluble complexes Depletion Zone Al-P Cation-phosphate complexes are relatively insoluble and immobile in soil; these include oxides and hydroxides of Al and Fe Mg-P Fe-P Ca-P Plants don’t take up organic phosphate Organic phosphates Roots growing in 31P-labeled soil. Only P immediately next to roots is taken up 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

15. Root system architecture can optimize foraging for phosphate • 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 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.

16. Potassium: Potash, from the ashes in the pot Potassium is an essential macronutrient Enhances fertility Maintains turgor and reduces wilting Promotes stress tolerance Regulates stomatal conductance, photosynthesis and transpiration Regulates enzyme activities Symptomsof potassium deficiency Strengthens cell walls Maintains ionic balance Stimulates photosynthate translocation [K+] in soil = ~0.1 – 1 mM [K+] in plant cell cytoplasm = ~100 mM 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.

17. K+ mobilization is critical for K+ use efficiency As K+ becomes limiting, it becomes preferentially allocated to the cytosol Cytosol Vac. Prioritized K+ can be remobilized from less essential tissues into prioritized tissues such as growing and photosynthetic tissues Non-Prioritized 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.

18. Sulfur: Clean air can lead to deficient plants Until recently, sulfur dioxide emission from fossil fuel combustion led to acid rain and extensive damage to vulnerable plants Sulfur dioxide damage Eliminating S from air pollution uncovered crop plant deficiencies, particularly in oilseed rape and wheat 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.

19. Sulfur is an essential macronutrient in amino acids & other compounds Flavor or odor Amino acids HS-CH2-CH-COOH NH2 S S Allicin (garlic flavor) O Cysteine (Cys) S S SH Allyl-isothiocyanate (horseradish flavor) Mercapto-p-menthan-3-one (blackcurrant) H3C-S-CH2-CH2-CH-COOH NH2 Methionine (Met) Defense S Oxidation /reduction, metal transport and detox S Glucosinolates are anti-herbivores S Camalexin is a defense compound induced by pathogens Glutathione Glutathione is an amino acid derivative involved in Redox reactions Cys 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

20. Magnesium: The “forgotten element” Mg in solution is a divalent cation Mg2+ Soil magnesium is a result of rock weathering and Mg2+ from seawater The Dolomite Mountains are named for the mineral dolomite MgCO3*CaCO3 Serpentine 3MgO*2SiO2*2H2O Magnesite MgCO3 Didier Descouens; Ra’ike; chensiyuan; James St. John

21. Magnesium is a cofactor for many enzymes and central to chlorophyll Mg2+ is a counter ion for the negative charges of ATP Mg2+ is an essential activator for many enzymes including Rubisco Mg2+ stabilizes ribosome 3D structure Mg2+ is central to chlorophyll Jensen, R.G. (2000). Activation of Rubisco regulates photosynthesis at high temperature and CO2. Proc. Natl. Acad. Sci. USA 97: 12937-12938.

22. Calcium: Low free cytosolic levels & functions in apoplast / vacuole Calcium stabilizes pectin in middle lamella of cell walls Middle lamella Cytosolic Ca2+ oscillations are second messengers in diverse responses Primary wall Secondary wall 2 μm 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 and adaptation 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.

23. Calcium deficiency causes cell wall defects and sometimes cell death 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 is translocated in the xylem (apoplast) but not the phloem (symplast), meaning that it cannot be remobilized when external supplies are limited Ca2+ 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

24. 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