title: Effects of potassium and sodium supply on drought-adaptive mechanisms in Eucalyptus grandis plantations.
abstract: A basic understanding of nutrition effects on the mechanisms involved in tree response to drought is essential under a future drier climate. A large-scale throughfall exclusion experiment was set up in Brazil to gain an insight into the effects of potassium (K) and sodium (Na) nutrition on tree structural and physiological adjustments to water deficit. Regardless of the water supply, K and Na supply greatly increased growth and leaf area index (LAI) of Eucalyptus grandis trees over the first 3 yr after planting. Excluding 37% of throughfall reduced above-ground biomass accumulation in the third year after planting for K- supplied trees only. E. grandis trees were scarcely sensitive to drought as a result of the utilization of water stored in deep soil layers after clear-cutting the previous plantation. Trees coped with water restriction through stomatal closure (isohydrodynamic behavior), osmotic adjustment and decrease in LAI. Additionally, droughted trees showed higher phloem sap sugar concentrations. K and Na supply increased maximum stomatal conductance, and the high water requirements of fertilized trees increased water stress during dry periods. Fertilization regimes should be revisited in a future drier climate in order to find the right balance between improving tree growth and limiting water shortage.
authors.affiliation: Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, CEP 13400-970, Piracicaba, SP, Brazil.
authors.forename: Patricia
authors.initials: P
authors.lastname: Battie-Laclau
authors.affiliation: CIRAD, UMR Eco&Sols, 2 Place Viala, 34060, Montpellier, France.|Departamento de Ciência Florestal, Universidade Estadual de São Paulo 'Júlio de Mesquita Filho', CEP 18610-300, Botucatu, SP, Brazil.|Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, CEP 13418-900, Piracicaba, SP, Brazil.
authors.forename: Jean-Paul
authors.initials: JP
authors.lastname: Laclau
authors.affiliation: Bordeaux Sciences Agro, INRA UMR 1391 ISPA, F-33170, Gradignan, France.|Nicholas School of the Environment, Duke University, Durham, NC, 27708, USA.
authors.forename: Jean-Christophe
authors.initials: JC
authors.lastname: Domec
authors.affiliation: CIRAD, UMR Eco&Sols, 2 Place Viala, 34060, Montpellier, France.|Montpellier SupAgro, 34060, Montpellier, France.
authors.forename: Mathias
authors.initials: M
authors.lastname: Christina
authors.affiliation: CIRAD, UMR Eco&Sols, 2 Place Viala, 34060, Montpellier, France.|Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, CEP 13418-900, Piracicaba, SP, Brazil.
authors.forename: Jean-Pierre
authors.initials: JP
authors.lastname: Bouillet
authors.affiliation: Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, CEP 13400-970, Piracicaba, SP, Brazil.
authors.forename: Marisa
authors.initials: M
authors.lastname: de Cassia Piccolo
authors.affiliation: Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, CEP 13418-900, Piracicaba, SP, Brazil.
authors.forename: José Leonardo
authors.initials: JL
authors.lastname: de Moraes Gonçalves
authors.affiliation: Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, CEP 13418-900, Piracicaba, SP, Brazil.
authors.forename: Rildo Moreira E
authors.initials: RME
authors.lastname: Moreira
authors.affiliation: Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, CEP 13400-970, Piracicaba, SP, Brazil.
authors.forename: Alex Vladimir
authors.initials: AV
authors.lastname: Krusche
authors.affiliation: CIRAD, UMR AGAP, Avenue Agropolis, 34398, Montpellier, France.
authors.forename: Jean-Marc
authors.initials: JM
authors.lastname: Bouvet
authors.affiliation: CIRAD, UMR Eco&Sols, 2 Place Viala, 34060, Montpellier, France.|Departamento de Ciências Atmosféricas, Universidade de São Paulo, CEP 05508-900, São Paulo, SP, Brazil.
authors.forename: Yann
authors.initials: Y
authors.lastname: Nouvellon
mesh_terms: D000222:Adaptation, Physiological / Q000187:drug effects*; D018533:Biomass; D001938:Brazil; D055864:Droughts; D005052:Eucalyptus / Q000187:drug effects / Q000254:growth & development / Q000502:physiology*; D052585:Phloem / Q000737:chemistry / Q000378:metabolism; D018515:Plant Leaves / Q000502:physiology; D054046:Plant Stomata / Q000502:physiology; D011188:Potassium / Q000494:pharmacology*; D012621:Seasons; D012964:Sodium / Q000494:pharmacology*; D012987:Soil
chemical_list: D012987:Soil; D012964:Sodium; D011188:Potassium
keywords: drought; eucalypt; nutrition; osmotic adjustment; rainfall exclusion; stomatal conductance; water deficit
references.citation: Almeida JCR, Laclau J-P, Gonçalves JLM, Ranger J, Saint-André L. 2010. A positive growth response to NaCl applications in Eucalyptus plantations established on K-deficient soils. Forest Ecology Management 259: 1786-1795.
references.citation: Arquero O, Barranco D, Benlloch M. 2006. Potassium starvation increases stomatal conductance in olive trees. HortScience 41: 433-436.
references.citation: Battie-Laclau P, Laclau J-P, Beri C, Mietton L, Muniz MA, Arenque BC, Piccolo MC, Jordan-Meille L, Bouillet J-P, Nouvellon Y. 2014. Photosynthetic and anatomical responses of Eucalyptus grandis leaves to potassium and sodium supply in a field experiment. Plant, Cell & Environment 37: 70-81.
references.citation: Battie-Laclau P, Laclau J-P, Piccolo MC, Arenque BC, Beri C, Mietton L, Muniz MRA, Jordan-Meille L, Buckeridge MS, Nouvellon Y et al. 2013. Influence of potassium and sodium nutrition on leaf area components in Eucalyptus grandis trees. Plant and Soil 371: 19-35.
references.citation: Benlloch-Gonzalez M, Arquero O, Fournier JM, Barranco D, Benlloch M. 2008. K+ starvation inhibits water-stress-induced stomatal closure. Journal of Plant Physiology 165: 623-630.
references.citation: Booth TH. 2013. Eucalypt plantations and climate change. Forest Ecology and Management 301: 28-34.
references.citation: Brando PM, Nepstad DC, Davidson EA, Trumbore SE, Ray D, Camargo P. 2008. Drought effects on litterfall, wood production and belowground carbon cycling in an Amazon forest: results of a throughfall reduction experiment. Philosophical Transactions of the Royal Society B 363: 1839-1848.
references.citation: Brown D, Rothery P. 1993. Models in biology: mathematics, statistics and computing. Chichester, UK: John Wiley & Sons Ltd.
references.citation: Cakmak I. 2005. The role of potassium in alleviating detrimental effects of abiotic stresses in plants. Journal of Plant Nutrition and Soil Science 168: 521-530.
references.citation: Cakmak I, Hengeler C, Marschner H. 1994. Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium-deficiency in bean-plants. Journal of Experimental Botany 45: 1251-1257.
references.citation: Callister AN, Arndt SK, Ades PK, Merchant A, Rowell D, Adams MA. 2008. Leaf osmotic potential of Eucalyptus hybrids responds differently to freezing and drought, with little clonal variation. Tree Physiology 28: 1297-1304.
references.citation: Cernusak LA, Arthur DJ, Pate JS, Farquhar GD. 2003. Water relations link carbon and oxygen isotope discrimination to phloem sap sugar concentration in Eucalyptus globulus. Plant Physiology 131: 1544-1554.
references.citation: Christina M, Laclau J-P, Gonçalves JLM, Jourdan C, Nouvellon Y, Bouillet J-P. 2011. Almost symmetrical vertical growth rates above and below ground in one of the world's most productive forests. Ecosphere 2: art 27.
references.citation: Clearwater MJ, Meinzer FC. 2001. Relationships between hydraulic architecture and leaf photosynthetic capacity in nitrogen-fertilized Eucalyptus grandis trees. Tree Physiology 21: 683-690.
references.citation: Clifford SC, Arndt SK, Corlett JE, Joshi S, Sankhla N, Popp M, Jones HG. 1998. The role of solute accumulation, osmotic adjustment and changes in cell wall elasticity in drought tolerance in Ziziphus mauritiana (Lamk.). Journal of Experimental Botany 49: 967-977.
references.citation: Cochrane TT, Cochrane TA. 2009. Differences in the way potassium chloride and sucrose solutions effect osmotic potential of significance to stomata aperture modulation. Plant Physiology and Biochemistry 47: 205-209.
references.citation: Cordell D, Drangert J-O, White S. 2009. The story of phosphorus: global food security and food for thought. Global Environmental Change 19: 292-305.
references.citation: Costa e Silva F, Shvaleva A, Maroco JP, Almeida MH, Chaves MM, Pereira JP. 2004. Responses to water stress in two Eucalyptus globulus clones differing in drought tolerance. Tree Physiology 24: 1165-1172.
references.citation: Darunsontaya T, Suddhiprakarn A, Kheoruenromne I, Prakongkep N, Gilkes RJ. 2012. The forms and availability to plants of soil potassium as related to mineralogy for upland Oxisols and Ultisols from Thailand. Geoderma 170: 11-24.
references.citation: Domec J-C, Palmroth S, Ward E, Maier CA, Thereuzien M, Oren R. 2009. Interactive effects of long term elevated CO2 and N-fertilization on the coordination between lead hydraulic conductance and stomatal conductance in Pinus taeda. Plant, Cell & Environment 32: 1500-1512.
references.citation: Dye PJ. 1996. Response of Eucalyptus grandis trees to soil water deficits. Tree Physiology 16: 233-238.
references.citation: Fatichi S, Leuzinger S, Korner C. 2014. Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytologist 201: 1086-1095.
references.citation: Fischer RA, Hsiao TC. 1968. Stomatal opening in isolated epidermal strips of Vicia faba II. Responses to KCI concentration and the role of potassium absorption. Plant Physiology 43: 1953-1958.
references.citation: Food and Agriculture Organization of the United Nations. 2010. Global forest resources assessment. Rome, Italy: FAO.
references.citation: Franks PJ, Drake PL, Froend RH. 2007. Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant, Cell & Environment 30: 19-30.
references.citation: Gajdanowicz P, Michard E, Sandmann M, Rocha M, Corrêa LG, Ramírez-Aguilar SJ, Gomez-Porras JL, González W, Thibaud JB, van Dongen JT et al. 2011. Potassium (K+) gradients serve as a mobile energy source in plant vascular tissues. Proceedings of the National Academy of Sciences, USA 108: 864-869.
references.citation: Gonçalves JLM, Alvares CA, Higa AR, Silva LD, Alfenas AC, Stahl J, Ferraz SFB, Lima WP, Brancalion PHS, Hubner A et al. 2013. Integrating genetic and silvicultural strategies to minimize abiotic and biotic constraints in Brazilian eucalypt plantations. Forest Ecology and Management 301: 6-27.
references.citation: Gundersen P, Andersen BR, Beier C, Rasmussen L. 1995. Experimental manipulations of water and nutrient input to a Norway spruce plantation at Klosterhede, Denmark I. Unintended physical and chemical changes by roof experiments. Plant and Soil 168-169: 601-611.
references.citation: Hartmann H, Ziegler W, Kolle O, Trumbore S. 2013. Thirst beats hunger - declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytologist 200: 340-349.
references.citation: Harwood C. 2011. Introductions: doing it right. In: Walker J, ed. Developing a Eucalypt resource. Learning from Australia and elsewhere. Christchurch, New Zealand: Wood Technology Research Centre, University of Canterbury, 43-54.
references.citation: IPCC. 2013. Stocker TF, Qin D, Plattner G-K, Tignor MMB, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM. eds. Climate change 2013: the physical science basis. Contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge, UK & New York, NY, USA: Cambridge University Press.
references.citation: Jin SH, Huang JQ, Li XQ, Zheng BS, Wu JS, Wang ZJ, Liu GH, Chen M. 2011. Effects of potassium supply on limitations of photosynthesis by mesophyll diffusion conductance in Carya cathayensis. Tree Physiology 31: 1142-1151.
references.citation: Johnson DW, DE Todd JR, Hanson PJ. 2008. Effects of throughfall manipulation on soil nutrient status: results of 12 years of sustained wet and dry treatments. Global Change Biology 14: 1661-1675.
references.citation: Klein T, Yakir D, Buchmann N, Grünzweig JM. 2014. Towards an advanced assessment of the hydrological vulnerability of forests to climate change-induced drought. New Phytologist 201: 712-716.
references.citation: Laclau J-P, Almeida JCR, Gonçalves JLM, Saint-André L, Ventura M, Ranger J, Moreira RM, Nouvellon Y. 2009. Influence of nitrogen and potassium fertilization on leaf lifespan and allocation of above-ground growth in Eucalyptus plantations. Tree Physiology 29: 111-124.
references.citation: Laclau J-P, Ranger J, Gonçalves JLM, Maquère V, Krusche AV, M'Bou AT, Nouvellon Y, Saint-André L, Bouillet J-P, Piccolo MC et al. 2010. Biogeochemical cycles of nutrients in tropical Eucalyptus plantations: main features shown by intensive monitoring in Congo and Brazil. Forest Ecology and Management 259: 1771-1785.
references.citation: Laclau J-P, Silva EA, Lambais G, Bernoux M, Le Maire G, Stape JL, Bouillet J-P, Gonçalves JLM, Jourdan C, Nouvellon Y. 2013. Dynamics of soil exploration by fine roots down to a depth of 10 m in Eucalyptus grandis plantations. Frontiers in Plant Science 4: art 243.
references.citation: Le Maire G, Marsden C, Verhoef W, Ponzoni FJ, Lo Seen D, Bégué A, Stape J-L, Nouvellon Y. 2011. Leaf area index estimation with MODIS reflectance time series and model inversion during full rotations of Eucalyptus plantations. Remote Sensing of Environment 115: 586-599.
references.citation: Lemcoff JH, Guarnaschelli AB, Garau A, Prystupa P. 2002. Elastic and osmotic adjustments in rooted cuttings of several clones of Eucalyptus camaldulensis Dehn. from southeastern Australia after a drought. Flora 197: 134-142.
references.citation: Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain JL, Laloi M, Coutos-Thévenot P, Maurousset L et al. 2013. Source-to-sink transport of sugar and regulation by environmental factors. Frontiers in Plant Science 4: 272.
references.citation: Limousin J-M, Rambal S, Ourcival J-M, Rodríguez-Calcerrada J, Pérez-Ramos IM, Rodríguez-Cortina R, Misson L, Joffre R. 2012. Morphological and phenological shoot plasticity in a Mediterranean evergreen oak facing long-term increased drought. Oecologia 169: 565-577.
references.citation: Manning DAC. 2010. Mineral sources of potassium for plant nutrition. Agronomy for Sustainable Development 30: 281-294.
references.citation: McDowell NG. 2011. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology 155: 1051-1059.
references.citation: McDowell NG, Fisher RA, Xu C, Domec JC, Hölttä T, Mackay DS, Sperry JS, Boutz A, Dickman L, Gehres N et al. 2013. Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework. New Phytologist 200: 304-321.
references.citation: McDowell NG, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG et al. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178: 719-739.
references.citation: Mengel K, Kirkby EA. 2001. Principles of plant nutrition, 5th edn. Dordrecht, the Netherlands: Kluwer Academic.
references.citation: Merchant A, Peuke AD, Keitel C, Macfarlane C, Warren CR, Adams MA. 2010. Phloem sap and leaf δ13C, carbohydrates, and amino acid concentrations in Eucalyptus globulus change systematically according to flooding and water deficit treatment. Journal of Experimental Botany 61: 1785-1793.
references.citation: Mitchell MPJ, O'Grady AP, Tissue DT, White DA, Ottenschlaeger ML, Pinkard EA. 2013. Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytologist 197: 862-872.
references.citation: Muller B, Pantin F, Génard M, Turc O, Freixes S, Piques M, Gibon Y. 2011. Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. Journal of Experimental Botany 62: 1715-1729.
references.citation: Oren R, Sperry JS, Katul GG, Pataki DE, Ewers BE, Phillips N, Schafer K. 1999. Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant, Cell & Environment 22: 1515-1526.
references.citation: Paquette A, Messier C. 2010. The role of plantations in managing the world's forests in the Anthropocene. Frontiers in Ecology and the Environment 8: 27-34.
references.citation: Pate J, Shedley E, Arthur D, Adams M. 1998. Spatial and temporal variations in phloem sap composition of plantation-grown Eucalyptus globulus. Oecologia 117: 312-322.
references.citation: Pita P, Pardos JA. 2001. Growth, leaf morphology, water use and tissue water relations of Eucalyptus globulus clones in response to water deficit. Tree Physiology 21: 599-607.
references.citation: Römheld V, Kirkby EA. 2010. Research on potassium in agriculture: needs and prospects. Plant and Soil 335: 155-180.
references.citation: Sala A, Woodruff DR, Meinzer FC. 2012. Carbon dynamics in trees: feast or famine? Tree Physiology 32: 764-775.
references.citation: Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garcia MN, Turner BL. 2012. Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. Journal of Ecology 100: 309-316.
references.citation: Scholander PF, Bradstreet ED, Hemmingsen EA, Hammel HT. 1965. Sap Pressure in Vascular Plants Negative hydrostatic pressure can be measured in plants. Science 148: 339-346.
references.citation: Stoneman GL, Crombie DS, Whitford K, Hingston FJ, Giles R, Portlock CC, Galbraith JH, Dimmock GM. 1996. Growth and water relations of Eucalyptus marginata (jarrah) stands in response to thinning and fertilization. Tree Physiology 16: 267-274.
references.citation: Subbarao GV, Ito O, Berry WL, Wheeler RM. 2003. Sodium: a functional plant nutrient. Critical Reviews in Plant Sciences 22: 391-416.
references.citation: Tomemori H, Hamamura K, Tanabe K. 2002. Interactive effects of sodium and potassium on the growth and photosynthesis of spinach and komatsuna. Plant Production Science 5: 281-285.
references.citation: Tyree MT, Jarvis PG. 1982. Water in tissues and cells. In: Lange OL, Nobel PS, Osmond CB, Ziegler H, eds. Physiological plant ecology. II. Water relations and carbon assimilation, encyclopedia of plant physiology, new series, vol 12B. Berlin, Germany: Springer, 37-77.
references.citation: Wakeel A, Farooq M, Qadir M, Schubert S. 2011. Potassium substitution by sodium in plants. Critical Reviews in Plant Sciences 30: 401-413.
references.citation: Wang M, Zheng Q, Shen Q, Guo S. 2013. The critical role of potassium in plant stress response. International Journal of Molecular Sciences 14: 7370-7390.
references.citation: Warren CR, Bleby T, Adams MA. 2007. Changes in gas exchange versus leaf solutes as a means to cope with summer drought in Eucalyptus marginata. Oecologia 154: 1-10.
references.citation: White DA, Battaglia M, Mendham DS, Crombie DS, Kinal J, McGrath JF. 2010. Observed and modelled leaf area index in Eucalyptus globulus plantations: tests of optimality and equilibrium hypotheses. Tree Physiology 30: 831-844.
references.citation: White DA, Beadle CL, Worledge D. 1996. Leaf water relations of Eucalyptus globulus and E. nitens: seasonal, drought and species effects. Tree Physiology 16: 469-476.
references.citation: White DA, Crombie DS, Kinal J, Battaglia M, McGrath JF, Mendham DS, Walker SN. 2009. Managing productivity and drought risk in Eucalyptus globulus plantations in south-western Australia. Forest Ecology and Management 259: 33-44.
references.citation: White DA, Turner NC, Galbraith JH. 2000. Leaf water relations and stomatal behavior of four allopatric Eucalyptus species planted in Mediterranean southwestern Australia. Tree Physiology 20: 1157-1165.
references.citation: Whitehead D, Beadle CL. 2004. Physiological regulation of productivity and water use in Eucalyptus: a review. Forest Ecology and Management 193: 113-140.
references.citation: Wu Z, Dijkstra P, Koch GW, Peñuelas J, Hungate BA. 2011. Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Global Change Biology 17: 927-942.