The number of ecometabolomic studies, which use metabolomic analyses to disentangle organisms' metabolic responses and acclimation to a changing environment, has grown exponentially in recent years. Here, we review the results and conclusions of ecometabolomic studies on the impacts of four main drivers of global change (increasing frequencies of drought episodes, heat stress, increasing atmospheric carbon dioxide (CO2) concentrations and increasing nitrogen (N) loads) on plant metabolism. Ecometabolomic studies of drought effects confirmed findings of previous target studies, in which most changes in metabolism are characterized by increased concentrations of soluble sugars and carbohydrate derivatives and frequently also by elevated concentrations of free amino acids. Secondary metabolites, especially flavonoids and terpenes, also commonly exhibited increased concentrations when drought intensified. Under heat and increasing N loads, soluble amino acids derived from glutamate and glutamine were the most responsive metabolites. Foliar metabolic responses to elevated atmospheric CO2 concentrations were dominated by greater production of monosaccharides and associated synthesis of secondary metabolites, such as terpenes, rather than secondary metabolites synthesized along longer sugar pathways involving N-rich precursor molecules, such as those formed from cyclic amino acids and along the shikimate pathway. We suggest that breeding for crop genotypes tolerant to drought and heat stress should be based on their capacity to increase the concentrations of C-rich compounds more than the concentrations of smaller N-rich molecules, such as amino acids. This could facilitate rapid and efficient stress response by reducing protein catabolism without compromising enzymatic capacity or increasing the requirement for re-transcription and de novo biosynthesis of proteins.

Centre de Recerca Ecològica i Aplicacions Forestals Institute 08193 Cerdanyola del vallès Spain

Department of Biology University of Antwerp 2610 Wilrijk Belgium

Department of Environmental Systems Science Eidgenössische Technische Hochschule Zürich 8092 Zürich Switzerland

Global Change Research Institute Czech Academy of Sciences Bělidla 986 4a CZ 60300 Brno Czech Republic

Spain National Research Council Global Ecology Unit CREAF CSIC UAB 08193 Bellaterra Spain

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Penuelas J., Sardans J. Ecological metabolomics. Chem. Ecol. 2009;25:305–309. doi: 10.1080/02757540903062517. DOI

Kucina V., Ekstron C.T., Anderson S.B., Nielsen J.K., Olsen C.E., Bak S. Identification of defense compounds in Barberea vulgaris against the Herbivore Phyllotreta nemorum by an ecometabolomic approach. Plant Physiol. 2009;151:1977–1990. doi: 10.1104/pp.109.136952. PubMed DOI PMC

Sardans J., Peñuelas J., Rivas-Ubach A. Ecological metabolomics as a proxy for organisms, populations, and species lifestyle: Current development and future challenges. Chemoecology. 2011;21:191–225. doi: 10.1007/s00049-011-0083-5. DOI

Rivas-Ubach A., Pérez-Trujillo M., Sardans J., Gargallo-Garriga A., Parella T., Penuelas J. Ecometabolomics: Optimized NMR-based method. Methods Ecol. Evol. 2013;4:464–473. doi: 10.1111/2041-210X.12028. DOI

Rivas-Ubach A., Peñuelas J., Hódar J.A., Oravec M., Tolic L.P., Urban O., Sardans J. We Are What We Eat: A Stoichiometric and Ecometabolomic Study of Caterpillars Feeding on Two Pine Subspecies of Pinus sylvestris. Int. J. Mol. Sci. 2018;20:59. doi: 10.3390/ijms20010059. PubMed DOI PMC

Allevato D.M., Kiyota E., Mazzafera P., Nixon K.C. Ecometabolomic Analysis of Wild Populations of Pilocarpus pennatifolius (Rutaceae) Using Unimodal Analyses. Front. Plant Sci. 2019;10:258. doi: 10.3389/fpls.2019.00258. PubMed DOI PMC

Ozawa R., Shiojiri K., Sabelis M.W., Takabayashi J. Maize plants sprayed with either jasmonic acid or its precursor, methyl linolenate, attract armyworm parasitoids, but the composition of attractants differs. Èntomol. Exp. Appl. 2008;129:189–199. doi: 10.1111/j.1570-7458.2008.00767.x. DOI

Llusià J., Penuelas J., Sardans J., Owen S.M. Niinemets, Ülo Measurement of volatile terpene emissions in 70 dominant vascular plant species in Hawaii: Aliens emit more than natives. Glob. Ecol. Biogeogr. 2010;19:863–874. doi: 10.1111/j.1466-8238.2010.00557.x. DOI

Gullberg J., Jonsson P., Nordstrom A., Sjöström M., Moritz T. Design of experiments: An efficient strategy to identify factors influencing extraction and derivatization of Arabidopsis thaliana samples in metabolomic studies with gas chromatography/mass spectrometry. Anal. Biochem. 2004;331:283–295. doi: 10.1016/j.ab.2004.04.037. PubMed DOI

Allwood J.W., Goodacre R. An introduction to liquid chromatographya mass spectrometry instrumentation applied in plant metabolomic analyses. Phytochem. Anal. 2010;21:33–47. doi: 10.1002/pca.1187. PubMed DOI

Jennings K.R. The changing impact of the collision-induced decomposition of ions on mass spectrometry. Int. J. Mass Spectrom. 2000;200:479–493. doi: 10.1016/S1387-3806(00)00325-0. DOI

Emwas A.-H., Roy R., McKay R., Tenori L., Saccenti E., Gowda G.A.N., Raftery D., AlAhmari F., Jaremko Ł., Jaremko M., et al. NMR Spectroscopy for Metabolomics Research. Metabolites. 2019;9:123. doi: 10.3390/metabo9070123. PubMed DOI PMC

Sousa Silva M., Cordeiro C., Roessner U., Figuereido A. Editorial: Metabolomics in crop research-current and emerging methodologies. Front. Plant Sci. 2019;10:1013. doi: 10.3389/fpls.2019.01013. PubMed DOI PMC

Lewis I.A., Schommer S.C., Hodis B., Robb K.A., Tonelli M., Westler W.M., Sussman M.R., Markley J.L. Method for Determining Molar Concentrations of Metabolites in Complex Solutions from Two-Dimensional1H−13C NMR Spectra. Anal. Chem. 2007;79:9385–9390. doi: 10.1021/ac071583z. PubMed DOI PMC

Viant M.R., Bearden D.W., Bundy J.G., Burton I.W., Collette T.W., Ekman E.R., Ezernieks V., Karakach T., Lin C.-Y., Rochfort S., et al. International NMR-Based Environmental Metabolomics Intercomparison Exercise. Environ. Sci. Technol. 2009;43:219–225. doi: 10.1021/es802198z. PubMed DOI

Khakimov B., Bak S., Engelsen S.B. High-throughput cereal metabolomics: Current analytical technologies, challenges, and perspectives. J. Cereal Sci. 2014;59:393–418. doi: 10.1016/j.jcs.2013.10.002. DOI

Zhuang J., Zhang J., Hou X., Wang F., Xiong F. Transcriptomic, Proteomic, Metabolomic and Functional Genomic Approaches for the Study of Abiotic Stress in Vegetable Crops. Crit. Rev. Plant Sci. 2014;33:225–237. doi: 10.1080/07352689.2014.870420. DOI

Aliferis K.A., Chrysayi-Takousbalides M. Metabolomics in pesticide research and development: Review and future perspectives. Metabolomics. 2011;7:35–53. doi: 10.1007/s11306-010-0231-x. DOI

Kumar M., Kuzhiumparambil U., Pernice M., Jiang Z., Ralph P. Metabolomics: An emerging frontier of systems biology in marine macrophytes. Algal Res. 2016;16:76–92. doi: 10.1016/j.algal.2016.02.033. DOI

Tugizimana F., Mhlongo M.I., Piater L.A., Dubery I.A. Metabolomics in Plant Priming Research: The Way Forward? Int. J. Mol. Sci. 2018;19:1759. doi: 10.3390/ijms19061759. PubMed DOI PMC

Kumari A., Das P., Parida A.K., Agarwal P.K. Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Front. Plant Sci. 2015;6:537. doi: 10.3389/fpls.2015.00537. PubMed DOI PMC

Gandhi S., Khushu S., Tripathi R.P. Current metabolomic methodologies and their application to thermal stress. Curr. Metabol. 2013;1:335–352. doi: 10.2174/2213235X01666131212230658. DOI

Jones O.A., Dias D.A., Callahan D., Kouremenos K.A., Beale D.J., Roessner U. The use of metabolomics in the study of metals in biological systems. Metallomics. 2015;7:29–38. doi: 10.1039/C4MT00123K. PubMed DOI

Paudel J.R., Amirizian A., Krosse S., Giddings J., Ismail S.A.A., Xia J., Gloer J.B., van Dam N.M., Bede J.C. Effect of atmopspheric carbon dioxide levels and nitrate fertilization on glucosinolate biosynthesis in mechanically damaged Arabidopsis plants. BMC Plant Biol. 2016;16:68. doi: 10.1186/s12870-016-0752-1. PubMed DOI PMC

Hu Y., Peuke A.D., Zhao X., Yan J., Li C. Effects of simulated atmospheric nitrogen deposition on foliar chemistry and physiology of hybrid poplar seedlings. Plant Physiol. Biochem. 2019;143:94–108. doi: 10.1016/j.plaphy.2019.08.023. PubMed DOI

De Souza A.P., Cocuron J.-C., Garcia A.C., Alonso A.P., Buckeridge M.S. Changes in whole-plant metabolism during the grain-filling stage in sorghum grown under elevated CO2 and drought. Plant Physiol. 2015;169:1755–1765. doi: 10.1104/pp.15.01054. PubMed DOI PMC

Austen N., Walker H.J., Lake J.A., Phoenix G.K., Cameron D.D. The Regulation of Plant Secondary Metabolism in Response to Abiotic Stress: Interactions Between Heat Shock and Elevated CO2. Front. Plant Sci. 2019;10:1463. doi: 10.3389/fpls.2019.01463. PubMed DOI PMC

Feng S., Fu Q. Expansion of global drylands under a warming climate. Atmos. Chem. Phys. Discuss. 2013;13:10081–10094. doi: 10.5194/acp-13-10081-2013. DOI

Huang J., Yu H., Guan X., Wang G., Guo R. Accelerated dryland expansion under climate change. Nat. Clim. Chang. 2015;6:166–171. doi: 10.1038/nclimate2837. DOI

Rivas-Ubach A., Sardans J., Pérez-Trujillo M., Estiarte M., Peñuelas J. Strong relationship between elemental sotichiometry and metabolome in plants. Proc. Nat. Acad. Sci. USA. 2012;109:4181–4186. doi: 10.1073/pnas.1116092109. PubMed DOI PMC

Rivas-Ubach A., Sardans J., Gargallo-Garriga A., Parella T., Perez-Trujillo M., Estiarte M., Penuelas J. Drought stress enhances folivory by shifting foliar metabolomes in Quercus ilex trees. New Phytol. 2014;27:874–885. doi: 10.1111/nph.12687. PubMed DOI

Ullah N., Yüce M., Gökçe Z.N.O., Budak H. Comparative metabolite profiling of drought stress in roots and leaves of seven Triticeae species. BMC Genom. 2017;18:969. doi: 10.1186/s12864-017-4321-2. PubMed DOI PMC

Shahbazy M., Moradi P., Ertaylan G., Zahraei A., Kompany-Zareh M. FTICR mass spectrometry-based multivariate analysis to explore distinctive metabolites and metabolic pathways: A comprehensive bioanalytical strategy toward time-course metabolic profiling of Thymus vulgaris plants responding to drought stress. Plant Sci. 2020;290:110257. doi: 10.1016/j.plantsci.2019.110257. PubMed DOI

Bianco R.L., Rieger M., Sung S.-J.S. Effect of drought on sorbitol and sucrose metabolism in sinks and sources of peach. Physiol. Plant. 2000;108:71–78. doi: 10.1034/j.1399-3054.2000.108001071.x. DOI

Chaves M.M., Marôco J., Pereira J., Chaves M.M. Understanding plant responses to drought from genes to the whole plant. Funct. Plant Boil. 2003;30:239–264. doi: 10.1071/FP02076. PubMed DOI

Shen B., Jensen R.G., Bohnert H.J. Mannitol Protects against Oxidation by Hydroxyl Radicals. Plant Physiol. 1997;115:527–532. doi: 10.1104/pp.115.2.527. PubMed DOI PMC

Llanes A., Andrade A., Alemano S., Luna V. Metabolomic Approach to Understand Plant Adaptations to Water and Salt Stress. Plant Metab. Regul. Under Env. Stress. 2018:133–144. doi: 10.1016/b978-0-12-812689-9.00006-6. DOI

Keunen E., Peshev D., Vangronsveld J., Ende W.V.D., Cuypers A. Plant sugars are crucial players in the oxidative challenge during abiotic stress: Extending the traditional concept. Plant Cell Environ. 2013;36:1242–1255. doi: 10.1111/pce.12061. PubMed DOI

Alvarez S., Marsh E.L., Schroeder S.G., Schachtman D. Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ. 2008;31:325–340. doi: 10.1111/j.1365-3040.2007.01770.x. PubMed DOI

Barchet G.L., Dauwe R., Guy R.D., Schroeder W., Soolanayakanahally R.Y., Campbell M.M., Mansfield S.D. Investigating the drought-stress response of hybrid poplar genotypes by metabolite profiling. Tree Physiol. 2013;34:1203–1219. doi: 10.1093/treephys/tpt080. PubMed DOI

Gargallo-Garriga A., Preece C., Sardans J., Oravec M., Urban O., Penuelas J. Root exudate metabolomes change under drought and show limited capacity for recovery. Sci. Rep. 2018;8:12696. doi: 10.1038/s41598-018-30150-0. PubMed DOI PMC

Nakabayashi R., Mori T., Saito K. Alteration of flavonoid accumulation under drought stress in Arabidopsis thaliana. Plant Signal. Behav. 2014;9:e29518. doi: 10.4161/psb.29518. PubMed DOI PMC

Pavli O.I., Vlachos C.E., Kalloniati C., Flemetakis E., Skaracis G.N. Metabolite profiling reveals the effect of drought on sorghum (Sorghum bicolor L. Moench) metabolism. Plant Omics J. 2013;6:371–376.

Hsiao T.C. Plant responses to water stress. Ann. Rev. Plant Physiol. 1973;24:519–570. doi: 10.1146/annurev.pp.24.060173.002511. DOI

Fathi A., Tari D.B. Effect of Drought Stress, and its Mechanism in Plants. Int. J. Life Sci. 2016;10:1–6. doi: 10.3126/ijls.v10i1.14509. DOI

Ahanger M.A., Gul F., Ahmad P., Akram N.A. Plant Metabolites and Regulation Under Environmental Stress. Elsevier BV; Amsterdam, The Netherlands: 2018. Environmental Stresses and Metabolomics—Deciphering the Role of Stress Responsive Metabolites; pp. 53–67.

Thompson J., Stewart C.R., Morris C.J. Changes in Amino Acid Content of Excised Leaves During Incubation I. The Effect of Water Content of Leaves and Atmospheric Oxygen Level. Plant Physiol. 1966;41:1578–1584. doi: 10.1104/pp.41.10.1578. PubMed DOI PMC

Zhang H., Murzello C., Sun Y., Kim M.-S., Xie X., Jeter R.M., Zak J.C., Dowd S.E., Pare P.W. Choline and Osmotic-Stress Tolerance Induced in Arabidopsis by the Soil Microbe Bacillus subtilis (GB03) Mol. Plant Microbe Interact. 2010;23:1097–1104. doi: 10.1094/MPMI-23-8-1097. PubMed DOI

Gou W., Tian L., Ruan Z., Zheng P., Chen F., Zhang J., Cui Z., Li Z., Gao M., Shi W., et al. Accumulation of choline and glycinebetaine and drought stress tolerance induced in maize (Zea mays) by three plant growth promoting rhizobacteria (PGPR) strains. Pak. J. Bot. 2015;47:581–586.

Hayat S., Hayat Q., Alyemeni M., Wani A.S., Pichtel J., Ahmad A. Role of proline under changing environments. Plant Signal. Behav. 2012;7:1456–1466. doi: 10.4161/psb.21949. PubMed DOI PMC

Chen T.H.H., Murata N. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr. Opin. Plant Boil. 2002;5:250–257. doi: 10.1016/S1369-5266(02)00255-8. PubMed DOI

Hamilton E.W., Heckathorn S.A. Mitochondrial Adaptations to NaCl. Complex I Is Protected by Antioxidants and Small Heat Shock Proteins, Whereas Complex II Is Protected by Proline and Betaine1. Plant Physiol. 2001;126:1266–1274. doi: 10.1104/pp.126.3.1266. PubMed DOI PMC

Perlikowski D., Czyżniejewski M., Marczak L., Augustyniak A., Kosmala A. Water Deficit Affects Primary Metabolism Differently in Two Lolium multiflorum/Festuca arundinacea Introgression Forms with a Distinct Capacity for Photosynthesis and Membrane Regeneration. Front. Plant Sci. 2016;7:17. doi: 10.3389/fpls.2016.01063. PubMed DOI PMC

Michaletti A., Naghavi M.R., Toorchi M., Zolla L., Rinalducci S. Metabolomics and proteomics reveal drought-stress responses of leaf tissues from spring-wheat. Sci. Rep. 2018;8:5710. doi: 10.1038/s41598-018-24012-y. PubMed DOI PMC

Mekonnen D.W., Flügge U.-I., Ludewig F. Gamma-aminobutyric acid depletion affects stomata closure and drought tolerance of Arabidopsis thaliana. Plant Sci. 2016;245:25–34. doi: 10.1016/j.plantsci.2016.01.005. PubMed DOI

Klem K., Gargallo-Garriga A., Rattanapichai W., Oravec M., Holub P., Veselá B., Sardans J., Peñuelas J., Urban O. Distinct Morphological, Physiological, and Biochemical Responses to Light Quality in Barley Leaves and Roots. Front. Plant Sci. 2019;10:1026. doi: 10.3389/fpls.2019.01026. PubMed DOI PMC

Parida A.K., Panda A., Rangani J. Metabolomics-Guided Elucidation of Abiotic Stress Tolerance Mechanisms in Plants. Plant Metab. Regul. Under Env. Stress. 2018:89–131. doi: 10.1016/b978-0-12-812689-9.00005-4. DOI

Hare P., Cress W., van Staden J. Proline synthesis and degradation: A model system for elucidating stress-related signal transduction. J. Exp. Bot. 1999;50:413–434. doi: 10.1093/jxb/50.333.413. DOI

Zinta G., AbcElgawad H., Peshev D., Weedon J.T., van den Ende W., Nijs I., Janssens I.A., Beemster G.T.S., Asard H. Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospherioc CO2. J. Exp. Bot. 2018;69:2159–2170. doi: 10.1093/jxb/ery055. PubMed DOI PMC

Yang L., Wen K.-S., Ruan X., Zhao Y.-X., Wei F., Wang Q. Response of Plant Secondary Metabolites to Environmental Factors. Molecules. 2018;23:762. doi: 10.3390/molecules23040762. PubMed DOI PMC

Mundim F.M., Pringle E.G. Whole-Plant Metabolic Allocation Under Water Stress. Front. Plant Sci. 2018;9:852. doi: 10.3389/fpls.2018.00852. PubMed DOI PMC

Miura K., Tada Y. Regulation of water, salinity, and cold stress responses by salicylic acid. Front. Plant Sci. 2014;5:1–12. doi: 10.3389/fpls.2014.00004. PubMed DOI PMC

Shan C., Liang Z. Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Sci. 2010;178:130–139. doi: 10.1016/j.plantsci.2009.11.002. DOI

Mahouachi J., Arbona V., Gómez-Cadenas A. Hormonal changes in papaya seedlings subjected to prograssive water stress in this halophyte. Plant Growth Regul. 2007;53:43–51. doi: 10.1007/s10725-007-9202-2. DOI

Kumar S., Pandey A.K. Chemistry and Biological Activities of Flavonoids: An Overview. Sci. World J. 2013:1–16. doi: 10.1155/2013/162750. PubMed DOI PMC

Intergovernmental Panel on Climate Change (IPCC) Climate Change 2007: Synthesis Report. World Meteorological Organization; Geneva, Switzerland: 2007. Fourth Assessment Report.

Nagarajan S., Jagadish S.V.K., Prasad A.H., Thomar A., Anand A., Pal M., Agarwal P. Local climate affects growth, yield and grain quality of aromatic and non-aromatic rice in northwestern India. Agric. Ecosyst. Environ. 2010;138:274–281. doi: 10.1016/j.agee.2010.05.012. DOI

Scafaro A.P., Haynes P.A., Atwell B.J. Physiological and molecular changes in Oryza meridionalis Ng., a heat-tolerant species of wild rice. J. Exp. Bot. 2010;61:191–202. doi: 10.1093/jxb/erp294. PubMed DOI PMC

Xu S., Li J., Zhang X., Wei H., Cui L. Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ. Exp. Bot. 2006;56:274–285. doi: 10.1016/j.envexpbot.2005.03.002. DOI

Foyer C.H., Noctor G. Redox Regulation in Photosynthetic Organisms: Signaling, Acclimation, and Practical Implications. Antioxid. Redox Signal. 2009;11:861–905. doi: 10.1089/ars.2008.2177. PubMed DOI

Suzuki N., Mittler R. Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction. Physiol. Plant. 2006;126:45–51. doi: 10.1111/j.0031-9317.2005.00582.x. DOI

Potters G., Pasternak T.P., Guisez Y., Palme K.J., Jansen M.A.K. Stress-induced mosphogenic responses: Growing out of trouble? Trends Plant Sci. 2007;12:98–105. doi: 10.1016/j.tplants.2007.01.004. PubMed DOI

Wedow J.M., Yendrek C.R., Mello T.R., Creste S., Martinez C.A., Ainsworth E.A. Metabolite, and transcript profiling of Guinea grass (Panicum maximum Jacq) response to elevated [CO2] and temperature. Metabolomics. 2019;15:51. doi: 10.1007/s11306-019-1511-8. PubMed DOI PMC

Qi X., Xu W., Zhang J., Guo R., Zhao M., Hu L., Wang H., Dong H., Li Y. Physiological characteristics and metabolomics of transgenic wheat containing the maize C4 phosphoenolpyruvate carboxylase (PEPC) gene under high temperature stress. Protoplasma. 2016;254:1017–1030. doi: 10.1007/s00709-016-1010-y. PubMed DOI

Carrow R.N. Summer Decline of Bentgrass Greens. Golf Course Manager; Louisville, KY, USA: 1996. pp. 51–56.

Huang B., Gao H. Growth and Carbohydrate Metabolism of Creeping Bentgrass Cultivars in Response to Increasing Temperatures. Crop. Sci. 2000;40:1115–1120. doi: 10.2135/cropsci2000.4041115x. DOI

Youngner V.B., Nudge F.J. Soil Temperature, Air Temperature, and Defoliation Effects on Growth and Nonstructural Carbohydrates of Kentucky Bluegrass1. Agron. J. 1907;68:257–260. doi: 10.2134/agronj1976.00021962006800020012x. DOI

Song S.Q., Lei Y.B., Tian X.R. Proline Metabolism and Cross-Tolerance to Salinity and Heat Stress in Germinating Wheat Seeds. Russ. J. Plant Physiol. 2005;52:793–800. doi: 10.1007/s11183-005-0117-3. DOI

Yue Y., Jiang H., Du J., Shi L., Bin Q., Yang X., Wang L. Variations in physiological response and expression profiles of proline metabolism-related genes and heat shock transcription factor genes in petunia subjected to heat stress. Sci. Hortic. 2019;258:108811. doi: 10.1016/j.scienta.2019.108811. DOI

Kishor P., Hong Z., Miao G.H., Hu C., Verma D. Overexpression of [delta]-Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants. Plant Physiol. 1995;108:1387–1394. doi: 10.1104/pp.108.4.1387. PubMed DOI PMC

Solomon A., Beer S., Waisel Y., Jones G.P., Paleg L.G. Effects of NaCl on the carboxylating activity of rubisco from Tamarix jordanis in the presence and absence of proline-related compatible solutes. Physiol. Plant. 1994;90:198–204. doi: 10.1111/j.1399-3054.1994.tb02211.x. DOI

Prasad K., Saradhi P.P. Effect of zinc on free radicals and proline in Brassica and Cajanus. Phytochemisty. 1995;39:45–47. doi: 10.1016/0031-9422(94)00919-k. DOI

Kumar D., Chattopadhyay S. Glutathione modulates the expression of heat shock proteins via the transcription factors BZIP10 and MYB21 in Arabidopsis. J. Exp. Bot. 2018;69:3729–3743. doi: 10.1093/jxb/ery166. PubMed DOI PMC

Kocsy G., Szalai G., Galiba G. Induction of Glutathione Synthesis and Glutathione Reductase Activity by Abiotic Stresses in Maize and Wheat. Sci. World J. 2002;2:1699–1705. doi: 10.1100/tsw.2002.812. PubMed DOI PMC

Locy R.D., Wu S.-J., Bisnette J., Barger T.W., McNabb D., Zik M., Fromm H., Singh N.K., Cherry J.H. Plant Tolerance to Abiotic Stresses in Agriculture: Role of Genetic Engineering. Springer Science and Business Media LLC; Berlin/Heidelberg, Germany: 2000. The Regulation of GABA Accumulation by Heat Stress in Arabidopsis; pp. 39–52.

Rao S.R., Ravishankar C. Enhanced catharanthine and vidoline production in suspension cultures of Catheranthus roseus by ultraviolet-B light. J. Mol. Signal. 2008;3:9–14. PubMed PMC

Yu K.-W., Murthy H.N., Hahn E.-J., Paek K.Y. Ginsenoside production by hairy root cultures of Panax ginseng: Influence of temperature and light quality. Biochem. Eng. J. 2005;23:53–56. doi: 10.1016/j.bej.2004.07.001. DOI

Chan L.K., Koay S.S., Boey P.L., Bhatt A. Effects of abiotic stress on biomass and anthocyanin production in cell cultures of Melastoma malabathricum. Boil. Res. 2010;43:127–135. doi: 10.4067/s0716-97602010000100014. PubMed DOI

Zobayed S.M.A., Afreen F., Kozai T. Temperature stress can alter the photosynthetic efficiency and secondary metabolite concentrations in St. John’s wort. Plant Physiol. Biochem. 2005;43:977–984. doi: 10.1016/j.plaphy.2005.07.013. PubMed DOI

Singsaas E.L. Terpenes and thermotolerance of photosynthesis. New Phytol. 2000;146:1–4.

Lichtenthaler H.K., Schwender J., Disch A., Rohmer M. Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Lett. 1997;400:271–274. doi: 10.1016/s0014-5793(96)01404-4. PubMed DOI

Henry L.K., Gutensohn M., Thomas S.T., Noel J.P., Duradeva N. Orthologs of archael isopentenyl phosphate kinase regulate terpenoid production in plants. Proc. Nat. Acad. Sci. USA. 2015;112:10050–10055. PubMed PMC

Sairam R., Tyagi A. Physiology and molecular biology of salinity stress tolerance in plants. Curr. Sci. 2014;86:407–421.

Peters G.P., Andrew R.M., Canadell J.G., Friedlingstein P., Jackson R.B., Korsbakken J.I., Le Quéré C., Peregon A. Carbon dioxide emissions continue to grow amidst slowly emerging climate policies. Nat. Clim. Change. 2019;10:3–6. doi: 10.1038/s41558-019-0659-6. DOI

Duval B.D., Blankinship J.C., Dijkstra P., Hungate B.A. Retracted Asticle: CO2 effects on plant nutrient concentration depend on plant functional group and available nitrogen: A meta-analysis. Plant Ecol. 2011;213:505–521. doi: 10.1007/s11258-011-9998-8. DOI

Jin J., Tang C., Sale P. The impact of elevated carbon dioxide on the phosphorus nutrition of plants: A review. Ann. Bot. 2015;116:987–999. doi: 10.1093/aob/mcv088. PubMed DOI PMC

Hatfield J.L., Dold C. Water-Use Efficiency: Advances and Challenges in a Changing Climate. Front. Plant Sci. 2019;10:103. doi: 10.3389/fpls.2019.00103. PubMed DOI PMC

Li X., Jal-Ahammed G., Li Z.X., Wei J.P., Shen C., Yan P., Zhang P.P., Han W.Y. Stimulation in primary and secondary metabolism by elevated carbon dioxide alters green tea quality in Camelia sinensis L. Sci. Rep. 2016;7:7937. PubMed PMC

Wenzel S., Cox P., Eyring V., Friedlingstein P. Projected land photosynthesis constrained by changes in the seasonal cycle of atmospheric CO2. Nature. 2016;538:499–501. doi: 10.1038/nature19772. PubMed DOI

Penuelas J., Estiarte M. Can elevated CO(2) affect secondary metabolism and ecosystem function? Trends Ecol. Evol. 1998;13:20–24. doi: 10.1016/s0169-5347(97)01235-4. PubMed DOI

Penuelas J., Estiarte M., Kimball B. Flavonoid Responses in Wheat Grown at Elevated CO2: Green Versus Senescent Leaves. Photosynthetica. 2000;37:615–619. doi: 10.1023/a:1007131827115. DOI

Peñuelas J., Fernández-Martínez M., Vallicrosa H., Maspons J., Zuccarini P., Carnicer J., Sanders T.G.M., Krüger I., Obersteiner M., Janssens I.A., et al. Increasing atmospheric CO2 concentrations correlate with declining nutritional status of European forests. Commun. Boil. 2020;3:1–11. doi: 10.1038/s42003-020-0839-y. PubMed DOI PMC

Peñuelas J., Janssens I.A., Ciais P., Obersteiner M., Sardans J. Anthropogenic global shifts in biospheric N and P concentrations and ratios and their impacts on biodiversity, ecosystem productivity, food security, and human Health. Global Change Biol. 2020 doi: 10.1111/gcb.14981. PubMed DOI

Lindroth R.L., Kinney K.K., Platz C.L. Responses of deciduous trees to elevated atmospheric CO2, productivity, phytochemistry and insect performance. Ecology. 1993;4:763–777.

Penuelas J., Estiarte M., Llusià J. Carbon-based Secondary Compounds at Elevated CO2. Photosynthetica. 1997;33:313–319. doi: 10.1023/a:1022120431279. DOI

Penuelas J., Llusià J. Effects of Carbon Dioxide, Water Supply, and Seasonality on Terpene Content and Emission by Rosmarinus officinalis. J. Chem. Ecol. 1997;23:979–993. doi: 10.1023/b:joec.0000006383.29650.d7. DOI

Penuelas J., Estiarte M. Trends in plant carbon concentration and plant demand for N throughout this century. Oecologia. 1996;109:69. doi: 10.1007/s004420050059. PubMed DOI

Holopainen J.K., Virjamo V., Ghimire R.P., Blande J.D., Julkunen-Tiitto R., Kivimäenpää M. Climate Change Effects on Secondary Compounds of Forest Trees in the Northern Hemisphere. Front. Plant Sci. 2018;9:1445. doi: 10.3389/fpls.2018.01445. PubMed DOI PMC

Koricheva J., Larsson S., Haukioja E., Keinänen M. Regulation of Woody Plant Secondary Metabolism by Resource Availability: Hypothesis Testing by Means of Meta-Analysis. Oikos. 1998;83:212. doi: 10.2307/3546833. DOI

Sobuj N., Virjamo V., Zhang Y., Nybakken L., Julkunen-Tiitto R. Impacts of elevated temperature and CO2 concentration on growth and phenolics in the sexually dimorphic Populus tremula (L.) Environ. Exp. Bot. 2018;146:34–44. doi: 10.1016/j.envexpbot.2017.08.003. DOI

Vanzo E., Jud W., Li Z., Albert A., Domagalska M.A., Ghirardo A., Niederbacher B., Frenzel J., Beemster G.T., Asard H., et al. Facing the Future: Effects of Short-Term Climate Extremes on Isoprene-Emitting and Nonemitting Poplar1. Plant Physiol. 2015;169:560–575. doi: 10.1104/pp.15.00871. PubMed DOI PMC

Nissinen K., Nybakken L., Virjamo V., Julkunen-Tiitto R. Slow-growing Salix repens (Salicaceae) benefits from changing climate. Environ. Exp. Bot. 2016;128:59–68. doi: 10.1016/j.envexpbot.2016.04.006. DOI

McKiernan A.B., O’Reilly-Wapstra J., Price C., Davies N., Potts B., Hovenden M.J. Stability of Plant Defensive Traits Among Populations in Two Eucalyptus Species Under Elevated Carbon Dioxide. J. Chem. Ecol. 2012;38:204–212. doi: 10.1007/s10886-012-0071-4. PubMed DOI

Randriamanana T.R., Nissinen K., Ovaskainen A., Lavola A., Peltola H., Albrectsen B., Julkunen-Tiitto R. Does fungal endophyte inoculation affect the responses of aspen seedlings to carbon dioxide enrichment? Fungal Ecol. 2018;33:24–31. doi: 10.1016/j.funeco.2017.12.002. DOI

Llusià J., Peñuelas J. Changes in terpene content and emission in potted Mediterranean woody plants under severe drought. Can. J. Bot. 1998;8:1366–1373.

Peñuelas J., Llusià J. BVOCs: Plant defense against climate warming? Trends Plant Sci. 2003;3:105–109. PubMed

Blanch J.S., Penuelas J., Sardans J., Llusià J. Drought, warming and soil fertilization effects on leaf volatile terpene concentrations in Pinus halepensis and Quercus ilex. Acta Physiol. Plant. 2008;31:207–218. doi: 10.1007/s11738-008-0221-z. DOI

Bustos-Segura C., Dillon S., Keszei A., Foley W.J., Kulheim C. Intraspecific diversity of terpenes of Eucalyptus camaldulensis (Myrtaceae) at a continental scale. Aust. J. Bot. 2017;65:257. doi: 10.1071/bt16183. DOI

Templer P.H., Pinder R., Goodale C.L. Effects of nitrogen deposition on greenhouse-gas fluxes for forests and grasslands of North America. Front. Ecol. Environ. 2012;10:547–553. doi: 10.1890/120055. DOI

Carter T.S., Clark C.M., Fenn M.E., Jovan S., Perakis S.S., Riddell J., Schaberg P.G., Greaver T.L., Hastings M.G. Mechanisms of nitrogen deposition effects on temperate forest lichens and trees. Ecosphere. 2017;8:e01717. doi: 10.1002/ecs2.1717. PubMed DOI PMC

Schmitz A., Sanders T.G.M., Bolte A., Bussotti F., Dirnböck T., Johnson J., Peñuelas J., Pollastrini M., Prescher A.-K., Sardans J., et al. Responses of forest ecosystems in Europe to decreasing nitrogen deposition. Environ. Pollut. 2018;244:980–994. doi: 10.1016/j.envpol.2018.09.101. PubMed DOI

Lassaletta L., Billen G., Grizzetti B., Anglade J., Garnier J. 50-year trends in nitrogen use efficiency of world cropping systems: The relationship between yield and nitrogen input to cropland. Environ. Res. Lett. 2014;9:105011. doi: 10.1088/1748-9326/9/10/105011. DOI

Bodirsky B.L., Müller C. Robust relationship between yields and nitrogen inputs indicates three ways to reduce nitrogen pollution. Environ. Res. Lett. 2014;9:111005. doi: 10.1088/1748-9326/9/11/111005. DOI

Larsen S.U., Jorgensen H., Bukh C., Schjoerring J.K. Green biorefining: Effect of nitrogen fertilization on protein yield, protein extractability and amino acid composition of tall fescue biomass. Ind. Crop. Prod. 2019;130:642–652. doi: 10.1016/j.indcrop.2019.01.016. DOI

Huhn G., Schulz H. Contents of free amino acids in Scots pine needles from field sites with different levels of nitrogen deposition. New Phytol. 1996;134:95–101. doi: 10.1111/j.1469-8137.1996.tb01149.x. DOI

Calanni J., Berg E., Wood M., Mangis D., Boyce R., Weathers W., Sievering H. Atmospheric nitrogen deposition at a conifer forest: Response of free amino acids in Engelmann spruce needles. Environ. Pollut. 1999;105:79–89. doi: 10.1016/s0269-7491(98)00202-4. DOI

Limpens J., Berendse F. Growth reduction of Sphagnum magellanicum subjected to high nitrogen deposition: The role of amino acid nitrogen concentration. Oecologia. 2003;135:339–345. doi: 10.1007/s00442-003-1224-5. PubMed DOI

Gent M.P.N. Effect of Genotype, Fertilization, and Season on Free Amino Acids in Leaves of Salad Greens Grown in High Tunnels. J. Plant Nutr. 2005;28:1103–1116. doi: 10.1081/pln-200062762. DOI

Ćustić M.H., Horvatić M., Pecina M. Nitrogen Fertilization Influences Protein Nutritional Quality in Red Head Chicory. J. Plant Nutr. 2009;32:598–609. doi: 10.1080/01904160802714987. DOI

Kanmegne G., Mbouobda H.D., Fotso-Mbakop C.N., Omokolo D.N. The influence of stock plant fertilization on tissue concentrations of nitrogen, carbohydrates, and amino acids and on the rooting of leaf stem cuttings of Cola anomala K. Schum (Malvaceae) New For. 2017;48:17–31.

Xu Y., Xiao H. Free amino acid concentrations and nitrogen isotope signatures in Pinus massaniana (Lamb.) needles of different ages for indicating atmospheric nitrogen deposition. Env. Pollut. 2017;221:180–190. PubMed

Nokerbekova N., Suleimenov Y.T., Zhapayev R. Influence of Fertilizing with Nitrogen Fertilizer on the Content of Amino Acids in Sweet Sorghum Grain. Agric. Food Sci. Res. 2018;5:64–67. doi: 10.20448/journal.512.2018.52.64.67. DOI

Wen G., Cambouris A.N., Ziadi N., Bertrand A., Khelifi M. Nitrogen Fertilization Effects on the Composition of Foliar Amino Acids of Russet Burbank Potato. Am. J. Potato Res. 2019;96:541–551. doi: 10.1007/s12230-019-09743-6. DOI

Olsen K.M., Slimestad R., Lea U.S., Brede C., Løvdal T., Ruoff P., Verheul M., Lillo C. Temperature and nitrogen effects on regulators and products of the flavonoid pathway: Experimental and kinetic model studies. Plant Cell Environ. 2009;32:286–299. doi: 10.1111/j.1365-3040.2008.01920.x. PubMed DOI

Allwood J.W., Chandra S., Xu Y., Dunn W.B., Correa E., Hopkins L., Goodacre R., Tobin A.K., Bowsher C. Profiling of spatial metabolite distributions in wheat leaves under normal and nitrate limiting conditions. Phytochemisty. 2015;115:99–111. doi: 10.1016/j.phytochem.2015.01.007. PubMed DOI PMC

Prinsi B., Espen L. Mineral nitrogen sources differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize. BMC Plant Boil. 2015;15:96. doi: 10.1186/s12870-015-0482-9. PubMed DOI PMC

Pietilä M., Lähdesmäki P., Pietiläinen P., Ferm A., Hytönen J., Pätilä A. High nitrogen deposition causes changes in amino acid concentrations and protein spectra in needles of the scots pine (Pinus sylvestris) Environ. Pollut. 1991;72:103–115. doi: 10.1016/0269-7491(91)90061-Z. PubMed DOI

Ann-Brittedfast T.N., Ericsson A., Nordén L.-G. Accumulation of amino acids in some boreal forest plants in response to increased nitrogen availability. New Phytol. 1994;126:137–143. doi: 10.1111/j.1469-8137.1994.tb07539.x. DOI

Cánovas F.M., Ávila C., Cantón F.J.R., Cañas R.A., De La Torre F. Ammonium assimilation and amino acid metabolism in conifers. J. Exp. Bot. 2007;58:2307–2318. doi: 10.1093/jxb/erm051. PubMed DOI

Nordin A., Näsholm T. Nitrogen storage forms in nine boreal understory plant species. Oecologia. 1997;110:487–492. doi: 10.1007/s004420050184. PubMed DOI

Britto D.T., Siddiqi M.Y., Glass A.D.M., Kronzucker H.J. Futile transmembrane NH4+ cycling: A cellular hypothesis to explain ammonium toxicity in plants. Proc. Natl. Acad. Sci. USA. 2001;98:4255–4258. doi: 10.1073/pnas.061034698. PubMed DOI PMC

Leaf metabolic traits reveal hidden dimensions of plant form and function

Single and interactive effects of variables associated with climate change on wheat metabolome