At the molecular level, folivory activity on plants has mainly been related to the foliar concentrations of nitrogen (N) and/or particular metabolites. We studied the responses of different nutrients and the whole metabolome of Quercus ilex to seasonal changes and to moderate field experimental conditions of drought, and how this drought may affect folivory activity, using stoichiometric and metabolomic techniques. Foliar potassium (K) concentrations increased in summer and consequently led to higher foliar K : phosphorus (P) and lower carbon (C) : K and N : K ratios. Foliar N : P ratios were not lowest in spring as expected by the growth rate hypothesis. Trees exposed to moderate drought presented higher concentrations of total sugars and phenolics and these trees also experienced more severe folivory attack. The foliar increases in K, sugars and antioxidant concentrations in summer, the driest Mediterranean season, indicated enhanced osmoprotection under natural drought conditions. Trees under moderate drought also presented higher concentrations of sugars and phenolics; a plant response to avoid water loss. These shifts in metabolism produced an indirect relationship between increased drought and folivory activity.

CREAF Cerdanyola del Vallès 08913 Catalonia Spain

CSIC Global Ecology Unit CREAF CEAB CSIC UAB Cerdanyola del Vallès 08913 Catalonia Spain

Global Change Research Centre Academy of Sciences of the Czech Republic Bĕlidla 4a CZ 603 00 Brno Czech Republic

Servei de Ressonància Magnètica Nuclear Faculty of Sciences and Biosciences Universitat Autònoma de Barcelona Bellaterra 08193 Barcelona Catalonia Spain

Zobrazit více v PubMed

Ali JG, Agrawal AA. 2012. Specialist versus generalist insect herbivores and plant defense. Trends in Plant Science 17: 293-302.

Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH et al. 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259: 660-684.

Anderegg WRL, Callaway ES. 2012. Infestation and hydraulic consequences of induced carbon starvation. Plant Physiology 159: 1866-1874.

Anderegg WRL, Kane JM, Anderegg LDL. 2013. Consequences of widespread tree mortality triggered by drought and temperature stress. Nature Climate Change 3: 30-36.

Anderson MJ, Gorley RN, Clarke KR. 2008. Permanova+ for PRIMER: guide to software and statistical methods. Plymouth, UK: Primer-E.

Arora A, Byrem TM, Nair MG, Strasburg GM. 2000. Modulation of liposomal membrane fluidity by flavonoids and isoflavonoids. Archives of Biochemistry and Biophysics 373: 102-109.

Babita M, Maheswari M, Rao LM, Shanker AK, Rao DG. 2010. Osmotic adjustment, drought tolerance and yield in castor (Ricinus communis L.) hybrids. Environmental and Experimental Botany 69: 243-249.

Barbeta A, Ogaya R, Peñuelas J. 2013. Dampening effects of long-term experimental drought on growth and mortality rates of a Holm oak forest. Global change biology 19: 3133-3144.

Bennett RN, Wallsgrove RM. 1994. Secondary metabolites in plant defense-mechanisms. New Phytologist 127: 617-633.

Berg TB. 2003. Catechin content and consumption ratio of the collared lemming. Oecologia 135: 242-249.

Bonal R, Munoz A, Maria Espelta J. 2010. Mismatch between the timing of oviposition and the seasonal optimum. The stochastic phenology of Mediterranean acorn weevils.. Ecological Entomology 35: 270-278.

Burda S, Oleszek W. 2001. Antioxidant and antiradical activities of flavonoids. Journal of Agricultural and Food Chemistry 49: 2774-2779.

Cakmak I. 2005. The role of potassium in alleviating detrimental effects of abiotic stresses in plants. Journal of Plant Nutrition and Soil Science-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde 168: 521-530.

Canadell J, Zedler P. 1995. Underground structures of woody plants in Mediterranean ecosystems of Australia, California and Chile. In: Ecology and biogeography of Mediterranean ecosystems in Chile, California and Australia. New York, NY, USA: Ecological Studies, Springer-Verlag, 108: 170-210.

Charlton AJ, Donarski JA, Harrison M, Jones SA, Godward J, Oehlschlager S, Arques JL, Ambrose M, Chinoy C, Mullineaux PM et al. 2008. Responses of the pea (Pisum sativum L.) leaf metabolome to drought stress assessed by nuclear magnetic resonance spectroscopy. Metabolomics 4: 312-327.

Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG et al. 2012. Global convergence in the vulnerability of forests to drought. Nature 491: 752-755.

Choong MF, Lucas PW, Ong JSY, Pereira B, Tan HTW, Turner IM. 1992. Leaf fracture-toughness and sclerophylly - their correlations and ecological implications. New Phytologist 121: 597-610.

Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F. 2000. Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences 57: 779-795.

Diaz Napal GN, Defago MT, Valladares GR, Palacios SM. 2010. Response of Epilachna paenulata to two flavonoids, pinocembrin and quercetin, in a comparative study. Journal of chemical ecology 36: 898-904.

Ehness R, Ecker M, Godt DE, Roitsch T. 1997. Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9: 1825-1841.

Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J et al. 2003. Growth rate-stoichiometry couplings in diverse biota. Ecology Letters 6: 936-943.

Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH. 1996. Organism size, life history, and N : P stoichiometry. BioScience 46: 674-684.

Fiehn O. 2002. Metabolomics - the link between genotypes and phenotypes. Plant Molecular Biology 48: 155-171.

Galiano L, Martinez-Vilalta J, Sabate S, Lloret F. 2012. Determinants of drought effects on crown condition and their relationship with depletion of carbon reserves in a Mediterranean holm oak forest. Tree Physiology 32: 478-489.

Grimaud F, Renaut J, Dumont E, Sergeant K, Lucau-Danila A, Blervacq A-S, Sellier H, Bahrman N, Lejeune-Henaut I, Delbreil B et al. 2013. Exploring chloroplastic changes related to chilling and freezing tolerance during cold acclimation of pea (Pisum sativum L.). Journal of Proteomics 80: 145-159.

Gusewell S, Koerselman M. 2002. Variation in nitrogen and phosphorus concentrations of wetland plants. Perspectives in Plant Ecology, Evolution and Systematics 5: 37-61.

Hare PD, Cress WA. 1997. Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation 21: 79-102.

Herms DA, Mattson WJ. 1992. The dilemma of plants - to grow or defend. Quarterly Review of Biology 67: 283-335.

Ingram J, Bartels D. 1996. The molecular basis of dehydration tolerance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 377-403.

IPCC. 2007. Core Writing Team, Pachauri RK, Reisinger A. Fourth Assessment Report: Climate change 2007 (AR4) Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva, Switzerland: IPCC.

James S. 1984. Lignotubers and burls - their structure, function and ecological significance in Mediterranean ecosystems. Botanical Review 50: 225-266.

Jansen JJ, Allwood JW, Marsden-Edwards E, van der Putten WH, Goodacre R, van Dam NM. 2009. Metabolomic analysis of the interaction between plants and herbivores. Metabolomics 5: 150-161.

Ji L-Z, An L-L, Wang X-W. 2011. Growth responses of gypsy moth larvae to elevated CO2: the influence of methods of insect rearing. Insect Science 18: 409-418.

Kessler A, Baldwin IT. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291: 2141-2144.

Khosravifar S, Yarnia M, Benam MBK, Moghbeli AHH. 2008. Effect of potassium on drought tolerance in potato cv. Agria. Journal of Food, Agriculture & Environment 6: 236-241.

t'Kindt R, De Veylder L, Storme M, Deforce D, Van Bocxlaer J. 2008. LC-MS metabolic profiling of Arabidopsis thaliana plant leaves and cell cultures: optimization of pre-LC-MS procedure parameters. Journal of Chromatography B-Analytical Technologies in the Biomedical and Life Sciences 871: 37-43.

Kosonen M, Keski-Saari S, Ruuhola T, Constabel CP, Julkunen-Tiitto R. 2012. Effects of overproduction of condensed ttannins and elevated temperature on chemical and ecological traits of genetically modified hybrid aspens (Populus tremula × P  tremuloides). Journal of chemical ecology 38: 1235-1246.

Landhausser SM, Lieffers VJ. 2002. Leaf area renewal, root retention and carbohydrate reserves in a clonal tree species following above-ground disturbance. Journal of Ecology 90: 658-665.

Larsson S. 1989. Stressful times for the plant stress - insect performance hypothesis. Oikos 56: 277-283.

Larsson S, Bjorkman C. 1993. Performance of chewing and phloem-feeding insects on stressed trees. Scandinavian Journal of Forest Research 8: 550-559.

Laus MN, Soccio M, Trono D, Liberatore MT, Pastore D. 2011. Activation of the plant mitochondrial potassium channel by free fatty acids and acyl-CoA esters: a possible defence mechanism in the response to hyperosmotic stress. Journal of Experimental Botany 62: 141-154.

Lee KG, Shibamoto T, Takeoka GR, Lee SE, Kim JH, Park BS. 2003. Inhibitory effects of plant-derived flavonoids and phenolic acids on malonaldehyde formation from ethyl arachidonate. Journal of Agricultural and Food Chemistry 51: 7203-7207.

Leiss KA, Choi YH, Abdel-Farid IB, Verpoorte R, Klinkhamer PGL. 2009. NMR metabolomics of thrips (Frankliniella occidentalis) resistance in Senecio hybrids. Journal of chemical ecology 35: 219-229.

Lindroth RL, Osier TL, Barnhill HRH, Wood SA. 2002. Effects of genotype and nutrient availability on phytochemistry of trembling aspen (Populus tremuloides Michx.) during leaf senescence. Biochemical Systematics and Ecology 30: 297-307.

Lokvam J, Kursar TA. 2005. Divergence in structure and activity of phenolic defenses in young leaves of two co-occurring Inga species. Journal of Chemical Ecology 31: 2563-2580.

Lugan R, Niogret M-F, Kervazo L, Larher FR, Kopka J, Bouchereau A. 2009. Metabolome and water status phenotyping of Arabidopsis under abiotic stress cues reveals new insight into ESK1 function. Plant, Cell & Environment 32: 95-108.

Martinez-Vilalta J, Pinol J. 2002. Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. Forest Ecology and Management 161: 247-256.

Matzek V, Vitousek PM. 2009. N : P stoichiometry and protein : RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecology Letters 12: 765-771.

McNeil SD, Nuccio ML, Ziemak MJ, Hanson AD. 2001. Enhanced synthesis of choline and glycine betaine in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferase. Proceedings of the National Academy of Sciences, USA 98: 10001-10005.

Munné-Bosch S, Peñuelas J. 2004. Drought-induced oxidative stress in strawberry tree (Arbutus unedo L.) growing in Mediterranean field conditions. Plant Science 166: 1105-1110.

Ogaya R, Peñuelas J. 2006. Contrasting foliar responses to drought in Quercus ilex and Phillyrea latifolia. Biologia Plantarum 50: 373-382.

Ogaya R, Peñuelas J. 2007. Tree growth, mortality, and above-ground biomass accumulation in a holm oak forest under a five-year experimental field drought. Plant Ecology 189: 291-299.

Ogaya R, Peñuelas J, Martinez-Vilalta J, Mangiron M. 2003. Effect of drought on diameter increment of Quercus ilex, Phillyrea latifolia, and Arbutus unedo in a holm oak forest of NE Spain. Forest Ecology and Management 180: 175-184.

Oleksyn J, Reich PB, Zytkowiak R, Karolewski P, Tjoelker MG. 2002. Needle nutrients in geographically diverse Pinus sylvestris L. populations. Annals of Forest Science 59: 1-18.

Passarinho JAP, Lamosa P, Baeta JP, Santos H, Ricardo CPP. 2006. Annual changes in the concentration of minerals and organic compounds of Quercus suber leaves. Physiologia Plantarum 127: 100-110.

Peñuelas J, Estiarte M. 1998. Can elevated CO2 affect secondary metabolism and ecosystem function? Trends in Ecology & Evolution 13: 20-24.

Peñuelas J, Munne-Bosch S, Llusia J, Filella I. 2004. Leaf reflectance and photo- and antioxidant protection in field-grown summer-stressed Phillyrea angustifolia. Optical signals of oxidative stress? New Phytologist 162: 115-124.

Peñuelas J, Sardans J. 2009a. Elementary factors. Nature 460: 803-804.

Peñuelas J, Sardans J. 2009b. Ecological metabolomics. Chemistry and Ecology 25: 305-309.

Peñuelas J, Sardans J, Estiarte M, Ogaya R, Carnicer J, Barbeta A, Rivas-Ubach A, Garbulsky M, Filella I. 2013a. Evidence of current impact of climate change on life: a walk from genes to the biosphere. Global Change Biology 19: 2303-2338.

Peñuelas J, Sardans J, Llusià J, Silva J, Owen S, Bala-Ola B, Linatoc AC, Dalimin MN, Niinemets Ü. 2013c. Foliar chemistry and standing folivory of early and late-successional species in a Bornean rainforest. Plant Ecology and Diversity 6: 245-256.

Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J et al. 2013b. Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications 4: 2934.

Pluskal T, Castillo S, Villar-Briones A, Oresic M. 2010. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics 11: doi: 10.1186/1471-2105-11-395.

Powell JA, Logan JA. 2005. Insect seasonality: circle map analysis of temperature-driven life cycles. Theoretical Population Biology 67: 161-179.

Price AH, Atherton NM, Hendry GAF. 1989. Plants under drought-stress generate activated oxygen. Free Radical Research Communications 8: 61-66.

R Development Core Team. 2011. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. ISBN 3-900051-07-0, URL http://www.R-project.org/.

Raffa KF, Powell EN, Townsend PA. 2013. Temperature-driven range expansion of an irruptive insect heightened by weakly coevolved plant defenses. Proceedings of the National Academy of Sciences, USA 110: 2193-2198.

Rani PU, Pratyusha S. 2013. Defensive role of Gossypium hirsutum L. anti-oxidative enzymes and phenolic acids in response to Spodoptera litura F. feeding. Journal of Asia-Pacific Entomology 16: 131-136.

Raubenheimer D, Simpson SJ. 2003. Nutrient balancing in grasshoppers: behavioural and physiological correlates of dietary breadth. Journal of Experimental Biology 206: 1669-1681.

RiceEvans CA, Miller J, Paganga G. 1997. Antioxidant properties of phenolic compounds. Trends in Plant Science 2: 152-159.

Rivas-Ubach A, Pérez-Trujillo M, Sardans J, Gargallo-Garriga A, Parella T, Peñuelas J. 2013. Ecometabolomics: optimized NMR-based method. Methods in Ecology and Evolution 4: 464-473.

Rivas-Ubach A, Sardans J, Pérez-Trujillo M, Estiarte M, Peñuelas J. 2012. Strong relationship between elemental stoichiometry and metabolome in plants. Proceedings of the National Academy of Sciences, USA 109: 4181-4186.

Rouault G, Candau J-N, Lieutier F, Nageleisen L-M, Martin J-C, Warzee N. 2006. Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe. Annals of Forest Science 63: 613-624.

Sardans J, Gargallo-Garriga A, Pérez-Trujillo M, Parella T, Seco R, Filella I, Peñuelas J. 2013a. Metabolic responses of Quercus ilex seedlings to wounding analysed with nuclear magnetic resonance. Plant Biology. doi:10.1111/plb.12032

Sardans J, Montes F, Peñuelas J. 2010. Determination of As, Cd, Cu, Hg and Pb in biological samples by modern electrothermal atomic absorption spectrometry. Spectrochimica Acta Part B-Atomic Spectroscopy 65: 97-112.

Sardans J, Peñuelas J. 2012. The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiology 160: 1741-1761.

Sardans J, Peñuelas J, Coll M, Vayreda J, Rivas-Ubach A. 2012a. Stoichiometry of potassium is largely determined by water availability and growth in Catalonian forests. Functional Ecology 26: 1077-1089.

Sardans J, Peñuelas J, Rivas-Ubach A. 2011b. Ecological metabolomics: overview of current developments and future challenges. Chemoecology 21: 191-225.

Sardans J, Rivas-Ubach A, Estiarte M, Ogaya R, Peñuelas J. 2013b. Field-simulated droughts affect elemental leaf stoichiometry in Mediterranean forests and shrublands. Acta Oecologica 50: 20-31.

Sardans J, Rivas-Ubach A, Peñuelas J. 2011a. Factors affecting nutrient concentration and stoichiometry of forest trees in Catalonia (NE Spain). Forest Ecology and Management 262: 2024-2034.

Sardans J, Rivas-Ubach A, Peñuelas J. 2012a. The C : N : P stoichiometry of organisms and ecosystems in a changing world: a review and perspectives. Perspectives in Plant Ecology, Evolution and Systematics 14: 33-47.

Sardans J, Rivas-Ubach A, Peñuelas J. 2012b. The elemental stoichiometry of aquatic and terrestrial ecosystems and its relationships with organismic lifestyle and ecosystem structure and function: a review and perspectives. Biogeochemistry 111: 1-39.

Spiess N, Oufir M, Matusikova I, Stierschneider M, Kopecky D, Homolka A, Burg K, Fluch S, Hausman J-F, Wilhelm E. 2012. Ecophysiological and transcriptomic responses of oak (Quercus robur) to long-term drought exposure and rewatering. Environmental and Experimental Botany 77: 117-126.

Sterner RW, Elser JJ. 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton, NJ, USA: Princeton University Press.

Strack D, Wray V, Harborne JB. 1994. The flavonoids, advances in research since 1986. Boca Raton, FL, USA: Chapman & Hall.

Treutter D. 2006. Significance of flavonoids in plant resistance: a review. Environmental Chemistry Letters 4: 147-157.

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.

White TCR. 1984. The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63: 90-105.

Widarto HT, Van Der Meijden E, Lefeber AWM, Erkelens C, Kim HK, Choi YH, Verpoorte R. 2006. Metabolomic differentiation of Brassica rapa following herbivory by different insect instars using two-dimensional nuclear magnetic resonance spectroscopy. Journal of chemical ecology 32: 2417-2428.

Williams WP, Davis FM, Buckley PM, Hedin PA, Baker GT, Luthe DS. 1998. Factors associated with resistance to fall armyworm (Lepidoptera: Noctuidae) and southwestern corn borer (Lepidoptera: Crambidae) in corn at different vegetative stages. Journal of Economic Entomology 91: 1471-1480.

Xu J, Li Y, Sun J, Du L, Zhang Y, Yu Q, Liu X. 2013. Comparative physiological and proteomic response to abrupt low temperature stress between two winter wheat cultivars differing in low temperature tolerance. Plant Biology 15: 292-303.

Amplified Drought Alters Leaf Litter Metabolome, Slows Down Litter Decomposition, and Modifies Home Field (Dis)Advantage in Three Mediterranean Forests

Ecometabolomics for a Better Understanding of Plant Responses and Acclimation to Abiotic Factors Linked to Global Change

We Are What We Eat: A Stoichiometric and Ecometabolomic Study of Caterpillars Feeding on Two Pine Subspecies of Pinus sylvestris

Root exudate metabolomes change under drought and show limited capacity for recovery

Close and distant: Contrasting the metabolism of two closely related subspecies of Scots pine under the effects of folivory and summer drought

Are the metabolomic responses to folivory of closely related plant species linked to macroevolutionary and plant-folivore coevolutionary processes?