Skip to main content
Log in

Ecological metabolomics: overview of current developments and future challenges

  • Review Paper
  • Published:
Chemoecology Aims and scope Submit manuscript

Abstract

Ecometabolomics, which aims to analyze the metabolome, the total number of metabolites and its shifts in response to environmental changes, is gaining importance in ecological studies because of the increasing use of new technical advances, such as modern HNMR spectrometers and GC-MS coupled to bioinformatic advances. We review here the state of the art and the perspectives of ecometabolomics. The studies available demonstrate ecometabolomic techniques have great sensitivity in detecting the phenotypic mechanisms and key molecules underlying organism responses to abiotic environmental changes to biotic interactions. But such studies are still scarce, and in most cases they are limited to the direct effects of a single abiotic factor or of biotic interactions between two trophic levels under controlled conditions. Several exciting challenges remain to be achieved through the use of ecometabolomics in field conditions, involving more than two trophic levels, or combining the effects of abiotic gradients with intra- and inter-specific relationships. The coupling of ecometabolomic studies with genomics, transcriptomics, ecosystem stoichiometry, community biology and biogeochemistry may provide a further step forward in many areas of ecological sciences, including stress responses, species lifestyle, life history variation, population structure, trophic interaction, nutrient cycling, ecological niche and global change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abdel-Farid IB, Jahangir M, van den Hondel C, Kim HK, Choi YH, Verpoorte R (2009) Fungal infection-induced metabolites in Brassica rapa. Plant Sci 176:608–615

    CAS  Google Scholar 

  • Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326

    PubMed  CAS  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    PubMed  CAS  Google Scholar 

  • Ali K, Maltese F, Zyprian E, Rex M, Choi YH, Verpoorte R (2009) NMR metabolic fingerprinting based identification of grapevine metabolites associated with downy mildew resistance. J Agr Food Chem 57:9599–9606

    CAS  Google Scholar 

  • Aliferis KA, Materzok S, Paziotou GN, Chrysayi-Tokousbalides M (2009) Lemna minor L. as a model organism for ecotoxicological studies performing H-1 NMR fingerprinting. Chemosphere 76:967–973

    PubMed  CAS  Google Scholar 

  • Allwood JW, Goodacre R (2009) An introduction to liquid chromatography-mass spectrometry instrumentation applied in plant metabolomic analyses. Phytochem Analysis 21:33–47

    Google Scholar 

  • Allwood JW, Ellis DI, Heald JK, Goodacre R, Mur LAJ (2006) Metabolomic approaches reveal that phosphatidic and phosphatidyl glycerol phospholipids are major discriminatory non-polar metabolites in responses by Brachypodium distachyon to challenge by Magnaporthe grisea. Plant J 46:351–368

    PubMed  CAS  Google Scholar 

  • Allwood JW, Ellis DI, Goodacre R (2008) Metabolomic technologies and their application to the study of plants and plant-host interactions. Physiol Plantarum 132:117–135

    CAS  Google Scholar 

  • Allwood JW, Clarke A, Goodacre R, Mur LAJ (2010) Dual metabolomics: a novel approach to understanding plant-pathogen interactions. Phytochemistry 71:590–597

    PubMed  Google Scholar 

  • Alvarez S, Marsh EL, Schroeder SG, Schachtman DP (2008) Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ 31:325–340

    PubMed  CAS  Google Scholar 

  • André A, Maucourt M, Moing A, Rolin D, Renaudin J (2005) Sugar import and phytopathogenicity of Spiroplasma citri: Glucose and fructose play distinct roles. Mol Plant Microbe Interact 18:33–42

    PubMed  Google Scholar 

  • Andreae MO, Crutzen PJ (1997) Atmospheric aerosols: biogeochemical sources and role in atmospheric chemistry. Science 276:1052–1058

    CAS  Google Scholar 

  • Arany AM, de Jong TJ, Kim HK, van Dam NM, Choi YH, Verpoorte R, van der Meijden E (2008) Glucosinolates and other metabolites in the leaves of Arabidopsis thaliana from natural populations and their effects on a generalist and a specialist herbivore. Chemoecology 18:65–71

    CAS  Google Scholar 

  • Bailey NJC, Oven M, Holmes E, Nicholson JK, Zenk MH (2003) Metabolomic analysis of the consequences of cadmium exposure in Silene cucubalus cell cultures via H-1 NMR spectroscopy and chemometrics. Phytochemistry 62:851–858

    PubMed  CAS  Google Scholar 

  • Barsch A, Tellstrom V, Patschkowski T, Kuster H, Niehaus K (2006) Metabolite profiles of nodulated alfalfa plants indicate that distinct stages of nodule organogenesis are accompanied by global physiological adaptations. Mol Plant Microbe Interact 19:998–1013

    PubMed  CAS  Google Scholar 

  • Bathellier C, Tcherkez G, Mauve C, Bligny R, Gout E, Ghashghaie J (2009) On the resilience of nitrogen assimilation by intact roots under starvation, as revealed by isotopic and metabolomic techniques. Rapid Commun Mass Sp 23:2847–2856

    CAS  Google Scholar 

  • Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J, Selbig J, Liu JL, Fernie AR, Sweetlove LJ (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 143:312–325

    PubMed  CAS  Google Scholar 

  • Bednarek P, Schneider B, Svatos A, Oldham NJ, Hahlbrock K (2005) Structural complexity, differential response to infection, and tissue specificity of indolic and phenylpropanoid secondary metabolism in Arabidopsis roots. Plant Physiol 138:1058–1070

    PubMed  CAS  Google Scholar 

  • Behrends V, Ryall B, Wang XZ, Bundy JG, Williams HD (2010) Metabolic profiling of Pseudomonas aeruginosa demonstrates that the anti-sigma factor MucA modulates osmotic stress tolerance. Mol Biosystems 6:562–569

    CAS  Google Scholar 

  • Biedrzycki ML, Bais HP (2009) Root secretions: from genes and molecules to microbial associations. J Exp Bot 60:1533–1534

    PubMed  CAS  Google Scholar 

  • Bino RJ, Hall RD, Fiehn O, Kopka J, Saito K, Draper J, Nikolau BJ, Mendes P, Roessner-Tunali U, Beale MH, Trethewey RN, Lange BM, Wurtele ES, Sumner LW (2004) Potential of metabolomics as a functional genomics tool. Trends Plant Sci 9:418–425

    PubMed  CAS  Google Scholar 

  • Bölling C, Fiehn O (2005) Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant Physiol 139:1995–2005

    PubMed  Google Scholar 

  • Bon D, Gilard V, Massou S, Peres G, Malet-Martino M, Martino R, Desmoulin F (2006) In vivo P-31 and H-1 HR-MAS NMR spectroscopy analysis of the unstarved Aporrectodea caliginosa (Lumbricidae). Biol Fert Soils 43:191–198

    CAS  Google Scholar 

  • Broeckling CD, Huhman DV, Farag MA, Smith JT, May GD, Mendes P, Dixon RA, Sumner LW (2005) Metabolic profiling of Medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitors on metabolism. J Exp Bot 56:323–336

    PubMed  CAS  Google Scholar 

  • Brosché M, Vinocur B, Alatalo ER, Lamminmäki A, Teichmann T, Ottow EA, Djilianov D, Afif D, Bogeat-Triboulot MB, Altman A, Polle A, Dreyer E, Rudd S, Lars P, Auvinen P, Kangasjärvi J (2005) Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert. Genome Biol 6:R:101

    Google Scholar 

  • Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Google Scholar 

  • Bundy JG, Osborn D, Weeks JM, Lindon JC, Nicholson JK (2001) An NMR-based metabonomic approach to the investigation of coelomic fluid biochemistry in earthworms under toxic stress. Febs Lett 500:31–35

    PubMed  CAS  Google Scholar 

  • Bundy JG, Lenz EM, Bailey NJ, Gavaghan CL, Svendsen C, Spurgeon D, Hankard PK, Osborn D, Weeks JA, Trauger SA (2002) Metabonomic assessment of toxicity of 4-fluoroaniline, 3,5-difluoroaniline and 2-fluoro-4-methylaniline to the earthworm Eisenia veneta (Rosa): identification of new endogenous biomarkers. Environ Toxicol Chem 21:1966–1972

    PubMed  CAS  Google Scholar 

  • Bundy JG, Ramlov H, Holmstrup M (2003) Multivariate metabolic profiling using H-1 nuclear magnetic resonance spectroscopy of freeze-tolerant and freeze-intolerant earthworms exposed to frost. Cryoletters 24:347–358

    PubMed  CAS  Google Scholar 

  • Bundy JG, Spurgeon DJ, Svendsen C, Hankard PK, Weeks JM, Osborn D, Lindon JC, Nicholson JK (2004) Environmental metabonomics: applying combination biomarker analysis in earthworms at a metal contaminated site. Ecotoxicology 13:797–806

    PubMed  CAS  Google Scholar 

  • Bundy JG, Keun HC, Sidhu JK, Spurgeon DJ, Svendsen C, Kille P, Morgan AJ (2007) Metabolic profile biomarkers of metal contamination in a sentinel terrestrial species are applicable across multiple sites. Environ Sci Technol 41:4458–4464

    PubMed  CAS  Google Scholar 

  • Bundy JG, Sidhu JK, Rana F, Spurgeon DJ, Svendsen C, Wren JF, Stürzenbaum SR, Morgan AJ, Kille P (2008) ‘Systems toxicology’ approach identifies coordinated metabolic responses to copper in a terrestrial non-model invertebrate, the earthworm Lumbricus rubellus. BMC Biol 6:25

    Google Scholar 

  • Bussell JA, Gidman EA, Causton DR, Gwynn-Jones D, Malham SK, Jones MLM, Reynolds B, Seed R (2008) Changes in the immune response and metabolic fingerprint of the mussel, Mytilus edulis (Linnaeus) in response to lowered salinity and physical stress. J Exp Mar Biol Ecol 358:78–85

    Google Scholar 

  • Cao M, Koulman A, Johnson LJ, Lane GA, Rasmussen S (2008) Advanced data-mining strategies for the analysis of direct-infusion ion trap mass spectrometry data from the association of perennial ryegrass with its endophytic fungus, Neotyphodium lolii. Plant Physiol 146:1501–1514

    PubMed  CAS  Google Scholar 

  • Carpenter JF, Crowe JH (1988) The mechanism of cryoprotection of proteins by solutes. Cryobiology 25:244–255

    PubMed  CAS  Google Scholar 

  • Cevallos–Cevallos JM, Rouseff R, Reyes-De-Corcuera J (2009) Untargeted metabolite analysis of healthy and Huanglongbing-infected orange leaves by CE-DAD. Electrophoresis 30:1240–1247

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Chiwocha S, Rouault G, Abrams S, von Aderkas P (2007) Parasitism of seed of Douglas fir (Pseudotsuga menziesii) by the seed chalcid, Megastigmus spermotrophus, and its influence on seed hormone physiology. Sex Plant Reprod 20:19–25

    CAS  Google Scholar 

  • Cho K, Shibato J, Agrawal GK, Jung YH, Kubo A, Jwa NS, Tamogami S, Satoh K, Kikuchi S, Higashi T, Kimura S, Saji H, Tanaka Y, Iwahashi H, Masuo Y, Rakwal R (2008) Integrated transcriptomics, proteomics, and metabolomics analyses to survey ozone responses in the leaves of rice seedling. J Proteome Res 7:2980–2998

    PubMed  CAS  Google Scholar 

  • Choi YH, Tapias EC, Kim HK, Lefeber AWM, Erkelens C, Verhoeven JTJ, Brzin J, Zel J, Verpoorte R (2004) Metabolic discrimination of Catharanthus roseus leaves infected by phytoplasma using H-1-NMR spectroscopy and multivariate data analysis. Plant Physiol 135:2398–2410

    PubMed  CAS  Google Scholar 

  • Choi YH, Kim HK, Linthorst HJM, Hollander JG, Lefeber AWM, Erkelens C, Nuzillard JM, Verpoorte R (2006) NMR metabolomics to revisit the tobacco mosaic virus infection in Nicotiana tabacum leaves. J Nat Prod 69:742–748

    PubMed  CAS  Google Scholar 

  • Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J 39:487–512

    PubMed  Google Scholar 

  • Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101:15243–15248

    PubMed  CAS  Google Scholar 

  • Copolovici LO, Filella I, Llusià J, Niinemets U, Peñuelas J (2005) The capacity for thermal protection of photosynthetic electron transport varies for different monoterpenes in Quercus ilex. Plant Physiol 139:485–496

    PubMed  CAS  Google Scholar 

  • Coucheney E, Daniell TJ, Chenu C, Nunan N (2008) Gas chromatographic metabolic profiling: a sensitive tool for functional microbial ecology. J Microbiol Meth 75:491–500

    CAS  Google Scholar 

  • Cramer GR, Ergül A, Grimplet J, Tillett RL, Tattersall EAR, Bohlman MC, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D, Schlauch KA, Schooley DA, Cushman JC (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomic 7:111–134

    CAS  Google Scholar 

  • Cyril J, Powell GL, Duncan RR, Baird WV (2002) Changes in membrane polar lipid fatty acids of Seashore paspalum in response to low temperature exposure. Crop Scie 42:2031–2037

    CAS  Google Scholar 

  • Davey MP, Burrell MM, Woodward FI, Quick WP (2008) Population-specific metabolic phenotypes of Arabidopsis lyrata ssp petraea. New Phytol 177:380–388

    PubMed  CAS  Google Scholar 

  • Davey MP, Woodward FI, Quick WP (2009) Intraspecfic variation in cold-temperature metabolic phenotypes of Arabidopsis lyrata ssp petraea. Metabolomics 5:138–149

    CAS  Google Scholar 

  • Degen T, Dillmann C, Marion-Poll F, Turlings TCJ (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135:1928–1938

    PubMed  CAS  Google Scholar 

  • Depuydt S, Trenkamp S, Fernie AR, Elftieh S, Renou JP, Vuylsteke M, Holsters M, Vereecke D (2009) An integrated genomics approach to define niche establishment by Rhodococcus fascians. Plant Physiol 149:1366–1386

    PubMed  CAS  Google Scholar 

  • Desbrosses GG, Kopka J, Udvardi MK (2005) Lotus japonicus metabolic profiling. Development of gas chromatography-mass spectrometry resources for the study of plant-microbe interactions. Plant Physiol 137:1302–1318

    PubMed  CAS  Google Scholar 

  • Dessureault-Rompre J, Nowack B, Schulin R, Luster J (2007) Spatial and temporal variation in organic acid anion exudation and nutrient anion uptake in the rhizosphere of Lupinus albus L. Plant Soil 301:123–134

    CAS  Google Scholar 

  • Ekman DR, Teng Q, Villeneuve DL, Kahl MD, Jensen KM, Durhan EJ, Ankley GT, Collette TW (2008) Investigating compensation and recovery of fathead minnow (Pimephales promelas) exposed to 17 alpha-ethynylestradiol with metabolite profiling. Environ Sci Technol 42:4188–4194

    PubMed  CAS  Google Scholar 

  • Ellis S, Mellor A (1995) Soils and environment. Routledge, London

    Google Scholar 

  • Feige U, Morimoto RI, Yahara I, Polla BS (1996) Stress-inducible cellular responses. Birkhauser Verlag, Basel

    Google Scholar 

  • Fernie AR, Trethewey RN, Krotzky AJ, Willmitzer L (2004) Metabolite profiling: from diagnostics to systems biology. Nat Rev Mol Cell Bio 5:763–769

    CAS  Google Scholar 

  • Ferreres F, Sousa C, Valentao P, Pereira JA, Seabra RM, Andrade PB (2007) Tronchuda cabbage flavonolds uptake by Pieris brassicae. Phytochemistry 68:361–367

    PubMed  CAS  Google Scholar 

  • Fiehn O (2002) Metabolomics––the link between genotypes and phenotypes. Plant Mol Biol 48:155–171

    PubMed  CAS  Google Scholar 

  • Fiehn O, Kopka J, Dormann P, Altmann T, Trethewey RN, Willmitzer L (2000) Metabolite profiling for plant functional genomics. Nature Biotechnol 18:1157–1161

    CAS  Google Scholar 

  • Fiehn O, Kloska S, Altmann T (2001) Integrated studies on plant biology using multiparallel techniques. Curr Opin Biotech 12:82–86

    PubMed  CAS  Google Scholar 

  • Figueiredo A, Fortes AM, Ferreira S, Sebastiana M, Choi YH, Sousa L, Acioli-Santos B, Pessoa F, Verpoorte R, Pais MS (2008) Transcriptional and metabolic profiling of grape (Vitis vinifera L.) leaves unravel possible innate resistance against pathogenic fungi. J Exp Bot 59:3371–3381

    PubMed  CAS  Google Scholar 

  • Filella I, Penuelas J (1999) Altitudinal differences in UV absorbance, UV reflectance and related morphological traits of Quercus ilex and Rhododendron ferrugineum in the Mediterranean region. Plant Ecol 145:157–165

    Google Scholar 

  • Filella I, Penuelas J, Llusia J (2006) Dynamics of the enhanced emissions of monoterpenes and methyl salicylate, and decreased uptake of formaldehyde, by Quercus ilex leaves after application of jasmonic acid. New Phytol 169:135–144

    PubMed  CAS  Google Scholar 

  • Filella I, Wilkinson MJ, Llusia J, Hewitt CN, Penuelas J (2007) Volatile organic compounds emissions in Norway spruce (Picea abies) in response to temperature changes. Physiol Plantarum 130:58–66

    CAS  Google Scholar 

  • Foito A, Byrne SL, Shepherd T, Stewart D, Barth S (2009) Transcriptional and metabolic profiles of Lolium perenne L. genotypes in response to a PEG-induced water stress. Plant Biotechnol J 7:719–732

    PubMed  CAS  Google Scholar 

  • Fridman E, Pichersky E (2005) Metabolomics, genomics, proteomics, and the identification of enzymes and their substrates and products. Curr Opinn Plant Biol 8:242–248

    CAS  Google Scholar 

  • Fukushima A, Kusano M, Nakamichi N, Kobayashi M, Hayashi N, Sakakibara H, Mizuno T, Saito K (2009a) Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proc Natl Acad Sci USA 106:7251–7256

    PubMed  CAS  Google Scholar 

  • Fukushima A, Kusano M, Redestig H, Arita M, Saito K (2009b) Integrated omics approaches in plant systems biology. Curr Opin Chem Biol 13:532–538

    PubMed  CAS  Google Scholar 

  • Fumagalli E, Baldoni E, Abbruscato P, Piffanelli P, Genga A, Lamanna R, Consonni R (2009) NMR techniques coupled with multivariate statistical analysis: tools to analyse Oryza sativa metabolic content under stress conditions. J Agron Crop Sci 195:77–88

    CAS  Google Scholar 

  • Gagneul D, Ainouche A, Duhaze C, Lugan R, Larher FR, Bouchereau A (2007) A reassessment of the function of the so-called compatible solutes in the halophytic Plumbaginaceae Limonium latifolium. Plant Physiol 144:1598–1611

    PubMed  CAS  Google Scholar 

  • Gaquerel E, Weinhold A, Baldwin IT (2009) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphigidae) and its natural host Nicotiana attenuata. VIII. An unbiased GCxGC-ToFMS analysis of the plant’s elicited volatile emissions. Plant Physiol 149:1408–1423

    PubMed  CAS  Google Scholar 

  • Gehlenborg N, O’Donoghue SI, Baliga NS, Goesmann A, Hibbs MA, Kitano H, Kohlbacher O, Neuweger H, Schneider R, Tenenbaum D, Gavin AC (2010) Visualization of omics data for systems biology. Nature Methods 7:S56–S68

    PubMed  CAS  Google Scholar 

  • Gibb JOT, Svendsen C, Weeks JM, Nicholson JK (1997) H-1 NMR spectroscopic investigations of tissue metabolite biomarker response to Cu(II) exposure in terrestrial invertebrates: identification of free histidine as a novel biomarker of exposure to copper in earthworms. Biomarkers 2:295–302

    CAS  Google Scholar 

  • Gidman EA, Goodacre R, Emmett B, Wilson DB, Carroll JA, Caporn SJM, Cresswell N, Gwynn-Jones D (2005) Metabolic fingerprinting for bio-indication of nitrogen responses in Calluna vulgaris heath communities. Metabolomics 1:279–285

    CAS  Google Scholar 

  • Gidman EA, Stevens CJ, Goodacre R, Broadhurst D, Emmett B, Gwynn-Jones D (2006) Using metabolic fingerprinting of plants for evaluating nitrogen deposition impacts on the landscape level. Global Change Biol 12:1460–1465

    Google Scholar 

  • Gong QQ, Li PH, Ma SS, Rupassara SI, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44:826–839

    PubMed  CAS  Google Scholar 

  • Gray GR, Heath D (2005) A global reorganization of the metabolome in Arabidopsis during cold acclimation is revealed by metabolic fingerprinting. Physiol Plantarum 124:236–248

    CAS  Google Scholar 

  • Griffin JL, Walker LA, Troke J, Osborn D, Shore RF, Nicholson JK (2000) The initial pathogenesis of cadmium induced renal toxicity. Febs Lett 478:147–150

    PubMed  CAS  Google Scholar 

  • Griffin JL, Walker L, Shore RF, Nicholson JK (2001) High-resolution magic angle spinning H-1-NMR spectroscopy studies on the renal biochemistry in the bank vole (Clethrionomys glareolus) and the effects of arsenic (As3+) toxicity. Xenobiotica 31:377–385

    PubMed  CAS  Google Scholar 

  • Gullberg J, Jonsson P, Nordström A, Sjöström M, Moritz T (2004) 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 331:283–295

    PubMed  CAS  Google Scholar 

  • Guo Q, Sidhu JK, Ebbels TMD, Rana F, Spurgeon DJ, Svendsen C, Sturzenbaum SR, Kille P, Morgan AJ, Bundy JG (2009) Validation of metabolomics for toxic mechanism of action screening with the earthworm Lumbricus rubellus. Metabolomics 5:72–83

    CAS  Google Scholar 

  • Haesler F, Hagn A, Frommberger M, Hertkorn N, Schmitt-Kopplin P, Munch JC, Schloter M (2008) In vitro antagonism of an actinobacterial Kitasatospora isolate against the plant pathogen Phytophthora citricola as elucidated with ultrahigh resolution mass spectrometry. J Microbiol Meth 75:188–195

    CAS  Google Scholar 

  • Hall RD (2006) Plant metabolomics: from holistic hope, to hype, to hot topic. New Phytol 169:453–468

    PubMed  CAS  Google Scholar 

  • Hamzehzarghani H, Kushalappa AC, Dion Y, Rioux S, Comeau A, Yaylayan V, Marshall WD, Mather DE (2005) Metabolic profiling and factor analysis to discriminate quantitative resistance in wheat cultivars against fusarium head blight. Physiol Mol Plant Pathol 66:119–133

    CAS  Google Scholar 

  • Hamzehzarghani H, Paranidharan V, Abu-Nada Y, Kushalappa AC, Dion Y, Rioux S, Comeau A, Yaylayan V, Marshall WD (2008) Metabolite profiling coupled with statistical analyses for potential high-throughput screening of quantitative resistance to fusarium head blight in wheat. Can J Plant Pathol (Revue Canadienne De Phytopathologie) 30:24–36

    CAS  Google Scholar 

  • Hansen BH, Altin D, Booth A, Vang SH, Frenzel M, Sorheim KR, Brakstad OG, Storseth TR (2010) Molecular effects of diethanolamine exposure on Calanus finmarchicus (Crustacea: Copepoda). Aquat Toxicol 99:212–222

    PubMed  CAS  Google Scholar 

  • Harm W (1980) Biological effects of ultraviolet radiation. Cambridge University Press, New York

    Google Scholar 

  • Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342

    PubMed  CAS  Google Scholar 

  • Harvey JA, van Dam NM, Gols R (2003) Interactions over four trophic levels: foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. J Anim Ecol 72:520–531

    Google Scholar 

  • Hendrawati O, Yao QQ, Kim HK, Linthorst HJM, Erkelens C, Lefeber AWM, Choi YH, Verpoorte R (2006) Metabolic differentiation of Arabidopsis treated with methyl jasmonate using nuclear magnetic resonance spectroscopy. Plant Sci 170:1118–1124

    CAS  Google Scholar 

  • Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F, Wu HC, Lara M, Town CD, Kopka J, Udvardi MK, Vance CP (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144:752–767

    PubMed  Google Scholar 

  • Hernández G, Valdés-Lépez O, Ramírez M, Goffard N, Weiller G, Aparicio-Fabre R, Fuentes SI, Erban A, Kopka J, Udvardi MK, Vance CP (2009) Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Physiol 151:1221–1238

    PubMed  Google Scholar 

  • Hines A, Oladiran GS, Bignell JP, Stentiford GD, Viant MR (2007) Direct sampling of organisms from the field and knowledge of their phenotype: key recommendations for environmental metabolomics. Environ Sci Technol 41:3375–3381

    PubMed  CAS  Google Scholar 

  • Hirai MY, Yano M, Goodenowe DB, Kanaya S, Kimura T, Awazuhara M, Arita M, Fujiwara T, Saito K (2004) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:10205–10210

    PubMed  CAS  Google Scholar 

  • Hirai MY, Klein M, Fujikawa Y, Yano M, Goodenowe DB, Yamazaki Y, Kanaya S, Nakamura Y, Kitayama M, Suzuki H, Sakurai N, Shibata D, Tokuhisa J, Reichelt M, Gershenzon J, Papenbrock J, Saito K (2005) Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J Biol Chem 280:25590–25595

    PubMed  CAS  Google Scholar 

  • Howarth JR, Parmar S, Jones J, Shepherd CE, Corol DI, Galster AM, Hawkins ND, Miller SJ, Baker JM, Verrier PJ, Ward JL, Beale MH, Barraclough PB, Hawkesford MJ (2008) Co-ordinated expression of amino acid metabolism in response to N and S deficiency during wheat grain filling. J Exp Bot 59:3675–3689

    PubMed  CAS  Google Scholar 

  • Huang CY, Roessner U, Eickmeier I, Genc Y, Callahan DL, Shirley N, Langridge P, Bacic A (2008) Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.). Plant Cell Physiol 49:691–703

    PubMed  CAS  Google Scholar 

  • Hughes RF, Uowolo A (2006) Impacts of Falcataria moluccana invasion on decomposition in Hawaiian lowland wet forests: the importance of stand-level controls. Ecosystems 9:977–991

    CAS  Google Scholar 

  • Hura T, Grzesiak S, Hura K, Thiemt E, Tokarz K, Wedzony M (2007) Physiological and biochemical tools useful in drought-tolerance detection in genotypes of winter triticale: accumulation of ferulic acid correlates with drought tolerance. Ann Bot London 100:767–775

    CAS  Google Scholar 

  • Huttunen L, Niemela P, Julkunen-Tiitto R, Heiska S, Tegelberg R, Rousi M, Kellomaki S (2008) Does defoliation induce chemical and morphological defenses in the leaves of silver birch seedlings under changing climate? Chemoecology 18:85–98

    CAS  Google Scholar 

  • Jagger J (1985) Solar-UV actions on living cells. Praefer Publishers, New York

    Google Scholar 

  • Jahangir M, Kim HK, Choi YH, Verpoorte R (2008) Metabolomic response of Brassica rapa submitted to pre-harvest bacterial contamination. Food Chem 107:362–368

    CAS  Google Scholar 

  • Janda T, Szalai G, Leskó K, Yordanova R, Apostol S, Popova LP (2007) Factors contributing to enhanced freezing tolerance in wheat during frost hardening in the light. Phytochemistry 68:1674–1682

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Jennings KR (2000) The changing impact of the collision-induced decomposition of ions on mass spectrometry. Int J Mass Spectrom 200:479–493

    CAS  Google Scholar 

  • Jobic C, Boisson AM, Gout E, Rascle C, Fèvre M, Cotton P, Bligny R (2007) Metabolic processes and carbon nutrient exchanges between host and pathogen sustain the disease development during sunflower infection by Sclerotinia sclerotiorum. Planta 226:251–265

    PubMed  CAS  Google Scholar 

  • Johnson HE, Broadhurst D, Goodacre R, Smith AR (2003) Metabolic fingerprinting of salt-stressed tomatoes. Phytochemistry 62:919–928

    PubMed  CAS  Google Scholar 

  • Jones AD, Hanley JC Jr, Stagliano MC, Appel H, Schultz JC (2006) Effect of insect herbivory and Pseudomonas syringae infection on secondary metabolite profiles in Arabidopsis thaliana leaves. In: Ward JL, Beale MH (eds) Proceedings from the 4th international plant metabolomics conference, pp 286. Metabolomics 2:269–334

    Google Scholar 

  • Jones OAH, Walker LA, Nicholson JK, Shore RF, Griffin JL (2007) Cellular acidosis in rodents exposed to cadmium is caused by adaptation of the tissue rather than an early effect of toxicity. Comp Biochem Phys D 2:316–321

    Google Scholar 

  • Jones OAH, Dondero F, Viarengo A, Griffin JL (2008a) Metabolic profiling of Mytilus galloprovincialis and its potential applications for pollution assessment. Mar Ecol Prog Ser 369:169–179

    CAS  Google Scholar 

  • Jones OAH, Spurgeon DJ, Svendsen C, Griffin JL (2008b) A metabolomics based approach to assessing the toxicity of the polyaromatic hydrocarbon pyrene to the earthworm Lumbricus rubellus. Chemosphere 71:601–609

    PubMed  CAS  Google Scholar 

  • Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714

    Google Scholar 

  • Kaiser KA, Barding GA, Larive CK (2009) A comparison of metabolite extraction strategies for H-1-NMR-based metabolic profiling using mature leaf tissue from the model plant Arabidopsis thaliana. Mag Reson Chem 47:S147–S156

    CAS  Google Scholar 

  • Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC (2004) Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135:483–495

    PubMed  CAS  Google Scholar 

  • Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168

    PubMed  CAS  Google Scholar 

  • Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50:967–981

    PubMed  CAS  Google Scholar 

  • Kaplan F, Badri DV, Zachariah C, Ajredini R, Sandoval FJ, Roje S, Levine LH, Zhang FL, Robinette SL, Alborn HT, Zhao W, Stadler M, Nimalendran R, Dossey AT, Bruschweiler R, Vivanco JM, Edison AS (2009) Bacterial attraction and quorum aensing inhibition in Caenorhabditis elegans exudates. J Chem Ecol 35:878–892

    PubMed  CAS  Google Scholar 

  • Kavouras IG, Mihalopoulos N, Stephanou EG (1998) Formation of atmospheric particles from organic acids produced by forests. Nature 395:683–686

    CAS  Google Scholar 

  • Keon J, Antoniw J, Carzaniga R, Deller S, Ward JL, Baker JM, Beale MH, Hammond-Kosack K, Rudd JJ (2007) Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host. Mol Plant Microbe Interact 20:178–193

    PubMed  CAS  Google Scholar 

  • Kikuchi J, Shinozaki K, Hirayama T (2004) Stable isotope labeling of Arabidopsis thaliana for an NMR-based metabolomics approach. Plant Cell Physiol 45:1099–1104

    PubMed  CAS  Google Scholar 

  • Kim HK, Verpoorte R (2010) Sample preparation for plant metabolomics. Phytochem Anal 21:4–13

    PubMed  CAS  Google Scholar 

  • Kim JK, Bamba T, Harada K, Fukusaki E, Kobayashi A (2007) Time-course metabolic profiling in Arabidopsis thaliana cell cultures after salt stress treatment. J Exp Bot 58:415–424

    PubMed  CAS  Google Scholar 

  • Kluender C, Sans-Piché F, Riedl J, Altenburger R, Härtig C, Laue G, Schmitt-Jansen M (2009) A metabolomics approach to assessing phytotoxic effects on the green alga Scenedesmus vacuolatus. Metabolomics 5:59–71

    CAS  Google Scholar 

  • Kontunen-Soppela S, Ossipov V, Ossipova S, Oksanen E (2007) Shift in birch leaf metabolome and carbon allocation during long-term open-field ozone exposure. Global Change Biol 13:1053–1067

    Google Scholar 

  • Kopka J, Fernie A, Weckwerth W, Gibon Y, Stitt M (2004) Metabolite profiling in plant biology: platforms and destinations. Genome Biol 5:109

    PubMed  Google Scholar 

  • Korn M, Gartner T, Erban A, Kopka J, Selbig J, Hincha DK (2010) Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol Plant 3:224–235

    PubMed  CAS  Google Scholar 

  • Kuzina V, Ekstrom CT, Andersen SB, Nielsen JK, Olsen CE, Bak S (2009) Identification of defense compounds in Barbarea vulgaris against the herbivore Phyllotreta nemorum by an ecometabolomic approach. Plant Physiol 151:1977–1990

    PubMed  CAS  Google Scholar 

  • Lake JA, Field KJ, Davey MP, Beerling DJ, Lomax BH (2009) Metabolomic and physiological responses reveal multi-phasic acclimation of Arabidopsis thaliana to chronic UV radiation. Plant Cell Environ 32:1377–1389

    PubMed  CAS  Google Scholar 

  • Larkindale J, Huang BR (2004) Changes of lipid composition and saturation level in leaves and roots for heat-stressed and heat-acclimated creeping bentgrass (Agrostis stolonifera). Environ Exp Bot 51:57–67

    CAS  Google Scholar 

  • Larrainzar E, Wienkoop S, Scherling C, Kempa S, Ladrera R, Arrese-Igor C, Weckwerth W, Gonzalez EM (2009) Carbon metabolism and bacteroid functioning are involved in the regulation of nitrogen fixation in Medicago truncatula under drought and recovery. Mol Plant Microbe Interact 22:1565–1576

    PubMed  CAS  Google Scholar 

  • Le Lay P, Isaure MP, Sarry JE, Kuhn L, Fayard B, Le Bail JL, Bastien O, Garin J, Roby C, Bourguignon-J (2006) Metabolomic, proteomic and biophysical analyses of Arabidopsis thaliana cells exposed to a caesium stress. Influence of potassium supply. Biochimie 88:1533–1547

    PubMed  CAS  Google Scholar 

  • Lee RE (1991) Principles of insect low temperature tolerance. In: Lee RE, Denlinger DL (eds) Insects at low temperatures. Champman & Hall, New York, pp 17–46

    Google Scholar 

  • Lei RH, Wu CQ, Yang BH, Ma HZ, Shi C, Wang QJ, Wang QX, Yuan Y, Liao MY (2008) Integrated metabolomic analysis of the nano-sized copper particle-induced hepatotoxicity and nephrotoxicity in rats: a rapid in vivo screening method for nanotoxicity. Toxicol Appl Pharm 232:292–301

    CAS  Google Scholar 

  • Leiss KA, Choi YH, Abdel-Farid IB, Verpoorte R, Klinkhamer PGL (2009a) NMR metabolomics of thrips (Frankliniella occidentalis) resistance in Senecio hybrids. J Chem Ecol 35:219–229

    PubMed  CAS  Google Scholar 

  • Leiss KA, Maltese F, Choi YH, Verpoorte R, Klinkhamer PGL (2009b) Identification of chlorogenic acid as a resistance factor for thrips in Chrysanthemum. Plant Physiol 150:1567–1575

    PubMed  CAS  Google Scholar 

  • Leiss KA, Choi YH, Verpoorte R, Klinkhamer PGL (2011) An overview of NMR metabolomic to identify secondary plant compounds involved in host plant resistance. Phytochem Rev 10:205–216

    Google Scholar 

  • Lenz EM, Hägele BF, Wilson ID, Simpson SJ (2001) High resolution H-1 NMR spectroscopic studies of the composition of the haemolymph of crowd- and solitary-reared nymphs of the desert locust, Schistocerca gregaria. Insect Biochem Molec 32:51–56

    CAS  Google Scholar 

  • Lewis IA, Schommer SC, Hodis B, Robb KA, Tonelli M, Westler WM, Sussman MR JLM (2007) Method for determining molar concentrations of metabolites in complex solutions from two-dimensional 1H–13C NMR spectra. Anal Chem 79:9385–9390

    PubMed  CAS  Google Scholar 

  • Li PH, Sioson A, Mane SP, Ulanov A, Grothaus G, Heath LS, Murali TM, Bohnert HJ, Grene R (2006) Response diversity of Arabidopsis thaliana ecotypes in elevated [CO2] in the field. Plant Mol Biol 62:593–609

    PubMed  CAS  Google Scholar 

  • Liang YS, Choi YH, Kim HK, Linthorst HJM, Verpoorte R (2006a) Metabolomic analysis of methyl jasmonate treated Brassica rapa leaves by 2-dimensional NMR spectroscopy. Phytochemistry 67:2503–2511

    PubMed  CAS  Google Scholar 

  • Liang YS, Kim HK, Lefeber AWM, Erkelens C, Choi YH, Verpoorte R (2006b) Identification of phenylpropanoids in methyl jasmonate treated Brassica rapa leaves using two-dimensional nuclear magnetic resonance spectroscopy. J Chromatogr A 1112:148–155

    PubMed  CAS  Google Scholar 

  • Lima MRM, Felgueiras ML, Graca G, Rodrigues JEA, Barros A, Gil AM, Dias ACP (2010) NMR metabolomics of esca disease-affected Vitis vinifera cv. Alvarinho leaves. J Exp Bot 61:4033–4042

    PubMed  CAS  Google Scholar 

  • Lindberg S, Banas A, Stymne S (2005) Effects of different cultivation temperatures on plasma membrane ATPase activity and lipid composition of sugar beet roots. Plant Physiol Bioch 43:261–268

    CAS  Google Scholar 

  • Lindon JC, Nicholson JK (2008) Spectroscopic and statistical techniques for information recovery in metabonomics and metabolomics. Annual Review of Anal Chem 1:45–69

    CAS  Google Scholar 

  • Lindon JC, Nicholson JK, Holmes E, Antti H, Bollard ME, Keun H, Beckonert O, Ebbels TM, Reilly MD, Robertson D, Stevens GJ, Luke P, Breau AP, Cantor GH, Bible RH, Niederhauser U, Senn H, Schlotterbeck G, Sidelmann UG, Laursen SM, Tymiak A, Car BD, Lehman-McKeeman L, Colet JM, Loukaci A, Thomas C (2003) Contemporary issues in toxicology––the role of metabonomics in toxicology and its evaluation by the COMET project. Toxicol Appl Pharm 187:137–146

    CAS  Google Scholar 

  • Llusia J, Peñuelas J (1999) Pinus halepensis and Quercus ilex terpene emission as affected by temperature and humidity. Biol Plantarum 42:317–320

    CAS  Google Scholar 

  • Llusia J, Peñuelas J (2001) Emission of volatile organic compounds by apple trees in response to spider mite attack and attraction of predatory mites. Exp Appl Acarology 25(1):65–77

    CAS  Google Scholar 

  • Llusia J, Peñuelas J, Alessio GA, Estiarte M (2008) Contrasting species-specific, compound-specific, seasonal, and interannual responses of foliar isoprenoid emissions to experimental drought in a mediterranean shrubland. Int J Plant Sci 169:637–645

    CAS  Google Scholar 

  • Llusia J, Peñuelas J, Sardans J, Owen SM, Niinemets U (2010) Measurement of volatile terpene emissions in 70 dominant vascular plant species in Hawaii: aliens emit more than natives. Global Ecol Biogeogr 19:863–874

    Google Scholar 

  • Lois R (1994) Accumulation of UV-absorbing flavonoids induced by UV-B radiation in Arabidopsis-thaliana L.1. Mechanisms of UV-resistance in Arabidopsis. Planta 194:498–503

    CAS  Google Scholar 

  • López-Gresa MP, Maltese F, Bellés JM, Conejero V, Kim HK, Choi YH, Verpoorte R (2010) Metabolic response of tomato leaves upon different plant-pathogen interactions. Phytochem Anal 21:89–94

    PubMed  Google Scholar 

  • Lowe RGT, Lord M, Rybak K, Trengove RD, Oliver RP, Solomon PS (2008) A metabolomic approach to dissecting osmotic stress in the wheat pathogen Stagonospora nodorum. Fungal Genet Biol 45:1479–1486

    PubMed  CAS  Google Scholar 

  • Lugan R, Niogret MF, 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 Environ 32:95–108

    PubMed  CAS  Google Scholar 

  • Lui L, Vikram A, Hamzehzarghani H, AC K (2005) Discrimination of three fungal diseases of potato tubers based on volatile metabolic profiles developed using GC/MS. Potato Res 48:85–96

    Google Scholar 

  • Lundberg P, Lundquist PO (2004) Primary metabolism in N-2-fixing Alnus incana-Frankia symbiotic root nodules studied with N-15 and P-31 nuclear magnetic resonance spectroscopy. Planta 219:661–672

    PubMed  CAS  Google Scholar 

  • Macel M, van Dam NM, Keurentjes JJB (2010) Metabolomics: the chemistry between ecology and genetics. Mol Ecol Resour 10:583–593

    PubMed  CAS  Google Scholar 

  • Malmendal A, Overgaard J, Bundy JG, Sorensen JG, Nielsen NC, Loeschcke V, Holmstrup M (2006) Metabolomic profiling of heat stress: hardening and recovery of homeostasis in Drosophila. Am J Physiol Reg I 291:R205–R212

    CAS  Google Scholar 

  • Mane SP, Robinet CV, Ulanov A, Schafleitner R, Tincopa L, Gaudin A, Nomberto G, Alvarado C, Solis C, Bolivar LA, Blas R, Ortega O, Solis J, Panta A, Rivera C, Samolski I, Carbajulca DH, Bonierbale M, Pati A, Heath LS, Bohnert HJ, Grene R (2008) Molecular and physiological adaptation to prolonged drought stress in the leaves of two Andean potato genotypes. Funct Plant Biol 35:669–688

    CAS  Google Scholar 

  • Maruyama K, Takeda M, Kidokoro S, Yamada K, Sakuma Y, Urano K, Fujita M, Yoshiwara K, Matsukura S, Morishita Y, Sasaki R, Suzuki H, Saito K, Shibata D, Shinozaki K, Yamaguchi-Shinozaki K (2009) Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol 150:1972–1980

    PubMed  CAS  Google Scholar 

  • McGarvery GB, Pocs R (2006) Metabolite profiling as a tool for investigation of the metabolic response of soybean infection by Phytophthora soja. In: Ward JL, Beale MH (eds) Proceedings from the 4th international plant metabolomics conference, pp 328. Metabolomics 2:269–334

    Google Scholar 

  • McKelvie JR, Yuk J, Xu YP, Simpson AJ, Simpson MJ (2009) H-1 NMR and GC/MS metabolomics of earthworm responses to sub-lethal DDT and endosulfan exposure. Metabolomics 5:84–94

    CAS  Google Scholar 

  • Micallef SA, Shiaris MP, Colón-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60:1729–1742

    PubMed  CAS  Google Scholar 

  • Michaud MR, Denlinger DL (2007) Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. J Comp Physol B 177:753–763

    CAS  Google Scholar 

  • Michaud MR, Benoit JB, López-Martínez G, Elnitsky MA, Lee RE, Denlinger DL (2008) Metabolomics reveals unique and shared metabolic changes in response to heat shock, freezing and desiccation in the Antarctic midge, Belgica antarctica. J Insect Physiol 54:645–655

    Google Scholar 

  • Miller GA, Islam MS, Claridge TDW, Dodgson T, Simpson SJ (2008) Swarm formation in the desert locust Schistocerca gregaria: isolation and NMR analysis of the primary maternal gregarizing agent. J Exp Biol 211:370–376

    PubMed  CAS  Google Scholar 

  • Mirnezhad M, Romero-González RR, Leiss KA, Choi YH, Verpoorte R, Klinkhamer PGL (2010) Metabolomic analysis of host plant resistance to thrips in wild and cultivated tomatoes. Phytochem Anal 21:110–117

    PubMed  CAS  Google Scholar 

  • Moalemiyan M, Vikram A, Kushalappa AC (2007) Detection and discrimination of two fungal diseases of mango (cv. Keitt) fruits based on volatile metabolite profiles using GC/MS. Postharvest Biol Tec 45:117–125

    CAS  Google Scholar 

  • Moco S, Bino RJ, De Vos RCH, Vervoort J (2007) Metabolomics technologies and metabolite identification. Trends Anal Chem 26:855–866

    CAS  Google Scholar 

  • Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19:417–422

    PubMed  Google Scholar 

  • Muth D, Kachlicki P, Krajewski P, Przystalski M, Stobiecki M (2009) Differential metabolic response of narrow leafed lupine (Lupinus angustifolius) leaves to infection with Colletotrichum lupini. Metabolomics 5:354–362

    CAS  Google Scholar 

  • Narasimhan K, Basheer C, Bajic VB, Swarup S (2003) Enhancement of plant-microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132:146–153

    PubMed  CAS  Google Scholar 

  • Nikiforova VJ, Gakière B, Kempa S, Adamik M, Willmitzer L, Hesse H, Hoefgen R (2004) Towards dissecting nutrient metabolism in plants: a systems biology case study on sulphur metabolism. J Exp Bot 55:1861–1870

    PubMed  CAS  Google Scholar 

  • Nikiforova VJ, Daub CO, Hesse H, Willmitzer L, Hoefgen R (2005a) Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response. J Exp Bot 56:1887–1896

    PubMed  CAS  Google Scholar 

  • Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005b) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138:304–318

    PubMed  CAS  Google Scholar 

  • Novotny AM, Schade JD, Hobbie SE, Kay AD, Kyle M, Reich PB, Elser JJ (2007) Stoichiometric response of nitrogen-fixing and non-fixing dicots to manipulations of CO2, nitrogen, and diversity. Oecologia 151:687–696

    PubMed  Google Scholar 

  • Oksman-Caldentey KM, Saito K (2005) Integrating genomics and metabolomics for engineering plant metabolic pathways. Curr Opin Biotech 16:174–179

    PubMed  CAS  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81

    PubMed  CAS  Google Scholar 

  • Ossipov V, Ossipova S, Bykov V, Oksanen E, Koricheva J, Haukioja E (2008) Application of metabolomics to genotype and phenotype discrimination of birch trees grown in a long-term open-field experiment. Metabolomics 4:39–51

    CAS  Google Scholar 

  • Overgaard J, Malmendal A, Sorensen JG, Bundy JG, Loeschcke V, Nielsen NC, Holmstrup M (2007) Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. J Insect Physiol 53:1218–1232

    PubMed  CAS  Google Scholar 

  • Ozawa R, Arimura G, Takabayashi J, Shimoda T, Nishioka T (2000) Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiol 41:391–398

    PubMed  CAS  Google Scholar 

  • Ozawa R, Shiojiri K, Sabelis MW, Takabayashi J (2008) Maize plants sprayed with either jasmonic acid or its precursor, methyl linolenate, attract armyworm parasitoids, but the composition of attractants differs. Entomol Exp Appl 129:189–199

    CAS  Google Scholar 

  • Paranidharan V, Abu-Nada Y, Hamzehzarghani H, Kushalappa AC, Mamer O, Dion Y, Rioux S, Comeau A, Choiniere L (2008) Resistance-related metabolites in wheat against Fusarium graminearum and the virulence factor deoxynivalenol (DON). Botany 86:1168–1179

    CAS  Google Scholar 

  • Parker D, Beckmann M, Zubair H, Enot DP, Caracuel-Rios Z, Overy DP, Snowdon S, Talbot NJ, Draper J (2009) Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea. Plant J 59:723–737

    PubMed  CAS  Google Scholar 

  • Paul C, Barofsky A, Vidoudez C, Pohnert G (2009) Diatom exudates influence metabolism and cell growth of co-cultured diatom species. Mar Ecol Prog Ser 389:61–70

    Google Scholar 

  • Peiris D, Dunn WB, Brown M, Kell DB, Roy I, Hedger JN (2008) Metabolite profiles of interacting mycelial fronts differ for pairings of the wood decay basidiomycete fungus, Stereum hirsutum with its competitors Coprinus micaceus and Coprinus disseminatus. Metabolomics 4:52–62

    CAS  Google Scholar 

  • Pena A, Teeling H, Huerta-Cepas J, Santos F, Yarza P, Brito-Echeverria J, Lucio M, Schmitt-Kopplin P, Meseguer I, Schenowitz C, Dossat C, Barbe V, Dopazo J, Rossello-Mora R, Schuler M, Glockner FO, Amann R, Gabaldon T, Anton J (2010) Fine-scale evolution: genomic, phenotypic and ecological differentiation in two coexisting Salinibacter ruber strains. Isme J 4:882–895

    PubMed  CAS  Google Scholar 

  • Peñuelas J, Llusia J (1997) Effects of carbon dioxide, water supply, and seasonality on terpene content and emission by Rosmarinus officinalis. J Chem Ecol 23:979–993

    Google Scholar 

  • Peñuelas J, Llusia J (1999) Short-term responses of terpene emission rates to experimental changes of PFD in Pinus halepensis and Quercus ilex in summer field conditions. Environ Exp Bot 42:61–68

    Google Scholar 

  • Peñuelas J, Llusia J (2001) The complexity of factors driving volatile organic compound emissions by plants. Biol Plantarum 44:481–487

    Google Scholar 

  • Peñuelas J, Llusia J (2003) BVOCs: plant defense against climate warming? Trends Plant Sci 8:105–109

    PubMed  Google Scholar 

  • Peñuelas J, Llusia J (2004) Plant VOC emissions: making use of the unavoidable. Trends Ecol Evol 19:402–404

    PubMed  Google Scholar 

  • Peñuelas J, Sardans J (2009a) Ecological metabolomics. Chem Ecol 25:305–309

    Google Scholar 

  • Peñuelas J, Sardans J (2009b) Elementary factors. Nature 460:803–804

    PubMed  Google Scholar 

  • Peñuelas J, Staudt M (2010) BVOCs and global change. Trend Plant Sci 15:133–144

    Google Scholar 

  • Peñuelas J, Llusià J, Estiarte M (1995) Terpenoids––a plant language. Trends Ecol Evol 10:289

    Google Scholar 

  • Peñuelas J, Idso SB, Ribas A, Kimball BA (1997) Effects of long-term atmospheric CO2 enrichment on the mineral concentration of Citrus aurantium leaves. New Phytol 135:439–444

    Google Scholar 

  • Peñuelas J, Llusià J, Gimeno BS (1999) Effects of ozone concentrations on biogenic volatile organic compounds emission in the Mediterranean region. Environ Pollut 105:17–23

    Google Scholar 

  • Peñuelas J, Filella I, Stefanescu C, Llusia J (2005a) Caterpillars of Euphydryas aurinia (Lepidoptera:Nymphalidae) feeding on Succisa pratensis leaves induce large foliar emissions of methanol. New Phytol 167:851–857

    PubMed  Google Scholar 

  • Peñuelas J, Llusia J, Asensio D, Munné-Bosch S (2005b) Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant Cell Environ 28:278–286

    Google Scholar 

  • Peñuelas J, Filella I, Seco R, Llusia J (2009a) Increase in isoprene and monoterpene emissions after re-watering of droughted Quercus ilex seedlings. Biol Plantarum 53:351–354

    Google Scholar 

  • Peñuelas J, Rutishauser T, Filella I (2009b) Phenology feedbacks on climate change. Science 324:887–888

    PubMed  Google Scholar 

  • Peñuelas J, Sardans J, Llusià J, Owen SM, Silva J, Niinemets U (2010) Higher allocation to low cost chemical defenses in invasive species of Hawaii. J Chem Ecol 36:1255–1270

    PubMed  Google Scholar 

  • Peñuelas J, Sardans J, Llusia J, Owen SM, Niinemets U (2011) Lower P contents and more widespread terpene presence in old Bornean than in young Hawaiian tropical plant species guilds. Ecosphere 2:1–19

    Google Scholar 

  • Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486

    PubMed  Google Scholar 

  • Pincetich CA, Viant MR, Hinton DE, Tjeerdema RS (2005) Metabolic changes in Japanese medaka (Oryzias latipes) during embryogenesis and hypoxia as determined by in vivo P-31 NMR. Comp Biochem Phys C 140:103–113

    Google Scholar 

  • Pinheiro C, Passarinho JA, Ricardo CP (2004) Effect of drought and rewatering on the metabolism of Lupinus albus organs. J Plant Physiol 161:1203–1210

    PubMed  CAS  Google Scholar 

  • Pluskal T, Nakamura T, Villar-Briones A, Yanagida M (2010) Metabolic profiling of the fission yeast S. pombe: quantification of compounds under different temperatures and genetic perturbation. Mol Biosyst 6:182–198

    PubMed  CAS  Google Scholar 

  • Poëssel JL, Sauge MH, Corre MN, Renaud C, Gaudillère M, Maucourt M, Deborde C, Dufour C, Loonis M, Lacroze JP, Pascal T, Moing A (2006) Metabolic profiling of shoot apices infested by the peach-potato aphid. In: Ward JL, Beale MH (eds) Proceedings from the 4th international plant metabolomics conference, pp 296. Metabolomics 2:269–334

    Google Scholar 

  • Prithiviraj B, Vikram A, Kushalappa AC, Yaylayan V (2004) Volatile metabolite profiling for the discrimination of onion bulbs infected by Erwinia carotovora ssp carotovora, Fusarium oxysporum and Botrytis allii. Eur J Plant Pathol 110:371–377

    CAS  Google Scholar 

  • Pungaliya C, Srinivasan J, Fox BW, Malik RU, Ludewig AH, Sternberg PW, Schroeder FC (2009) A shortcut to identifying small molecule signals that regulate behavior and development in Caenorhabditis elegans. Proc Natl Acad Sci USA 106:7708–7713

    PubMed  CAS  Google Scholar 

  • Rasmussen S, Parsons AJ, Fraser K, Xue H, Newman JA (2008) Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiol 146:1440–1453

    PubMed  CAS  Google Scholar 

  • Riipi M, Haukioja E, Lempa K, Ossipov V, Ossipova S, Pihlaja K (2004) Ranking of individual mountain birch trees in terms of leaf chemistry: seasonal and annual variation. Chemoecology 14:31–43

    CAS  Google Scholar 

  • Rizhsky L, Liang HJ, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

    PubMed  CAS  Google Scholar 

  • Robinson AR, Ukrainetz NK, Kang KY, Mansfield SD (2007) Metabolite profiling of Douglas-fir (Pseudotsuga menziesii) field trials reveals strong environmental and weak genetic variation. New Phytol 174:762–773

    PubMed  CAS  Google Scholar 

  • Rochfort SJ, Ezernieks V, Yen AL (2009) NMR-based metabolomics using earthworms as potential indicators for soil health. Metabolomics 5:95–107

    CAS  Google Scholar 

  • Roessner U, Patterson JH, Forbes MG, Fincher GB, Langridge P, Bacic A (2006) An investigation of boron toxicity in barley using metabolomics. Plant Physiol 142:1087–1101

    PubMed  CAS  Google Scholar 

  • Rosenblum ES, Viant MR, Braid BM, Moore JD, Friedman CS, Tjeerdema RS (2005) Characterizing the metabolic actions of natural stresses in the California red abalone, Haliotis rufescens using H-1 NMR metabolomics. Metabolomics 1:199–209

    CAS  Google Scholar 

  • Rosenblum ES, Tjeerdema RS, Viant MR (2006) Effects of temperature on host-pathogen-drug interactions in red abalone, Haliotis rufescens, determined by H-1 NMR metabolomics. Environ Sci Technol 40:7077–7084

    PubMed  CAS  Google Scholar 

  • Saito K, Matsuda F (2010) Metabolomics for functional genomics. systems biology, and biotechnology. Annu Rev Plant Biol 61:463–489

    PubMed  CAS  Google Scholar 

  • Samuelsson LM, Forlin L, Karlsson G, Adolfsson-Eric M, Larsson DGJ (2006) Using NMR metabolomics to identify responses of an environmental estrogen in blood plasma of fish. Aquat Toxicol 78:341–349

    PubMed  CAS  Google Scholar 

  • Sanchez DH, Szymanski J, Erban A, Udvardi MK, Kopka J (2010) Mining for robust transcriptional and metabolic responses to long-term salt stress: a case study on the model legume Lotus japonicus. Plant Cell Environ 33:468–480

    PubMed  CAS  Google Scholar 

  • Sardans J, Llusia J, Niinemets U, Owen S, Peñuelas J (2010) Foliar mono- and sesquiterpene contents in relation to leaf economic spectrum in native and alien species in Oahu (Hawai’i). J Chem Ecol 36:210–226

    PubMed  CAS  Google Scholar 

  • Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, Jourdain A, Bastien O, Fievet JB, Vailhen D, Amekraz B, Moulin C, Ezan E, Garin J, Bourguignon-J (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6:2180–2198

    PubMed  CAS  Google Scholar 

  • Scherling C, Roscher C, Giavalisco P, Schulze ED, Weckwerth W (2010) Metabolomics unravel contrasting effects of biodiversity on the performance of individual plant species. Plos One 5:e12569

    PubMed  Google Scholar 

  • Schlotterbeck G, Ceccarelli SM (2009) LC-SPE-NMR-MS: a total analysis system for bioanalysis. Bioanalysis 1:549–559

    PubMed  CAS  Google Scholar 

  • Schripsema J (2010) Application of NMR in plant metabolomics: techniques, problems and prospects. Phytochem Analysis 21:14–21

    CAS  Google Scholar 

  • Schroeder FC, del Campo ML, Grant JB, Weibel DB, Smedley SR, Bolton KL, Meinwald J, Eisner T (2006) Pinoresinol: a lignol of plant origin serving for defense in a caterpillar. Proc Natl Acad Sci USA 103:15497–15501

    PubMed  CAS  Google Scholar 

  • Sekiyama Y, Chikayama E, Kikuchi J (2010) Profiling polar and semipolar plant metabolites throughout extraction processes using a combined solution-state and high-resolution magic angle spinning NMR approach. Anal Chem 82:1643–1652

    PubMed  CAS  Google Scholar 

  • Semel Y, Schauer N, Roessner U, Zamir D, Fernie AR (2007) Metabolite analysis for the comparison of irrigated and non-irrigated field grown tomato of varying genotype. Metabolomics 3:289–295

    CAS  Google Scholar 

  • Shen B, Jensen RG, Bohnert HJ (1997) Increased resistance to oxidative stress in transgenic plants by targeting mannitol biosynthesis to chloroplasts. Plant Physiol 113:1177–1183

    PubMed  CAS  Google Scholar 

  • Simoh S, Quintana N, Kim HK, Choi YH, Verpoorte R (2009) Metabolic changes in Agrobacterium tumefaciens-infected Brassica rapa. J Plant Physiol 166:1005–1014

    PubMed  CAS  Google Scholar 

  • Smith AR, Johnson HE, Hall M (2003) Metabolic fingerprinting of salt-stresse tomatoes. Bulgarian J Plant Physiol Special Issue:153–163

  • Solanky KS, Burton IW, MacKinnon-SL, Walter JA, Dacanay A (2005) Metabolic changes in Atlantic salmon exposed to Aeromonas salmonicida detected by H-1-nuclear magnetic resonance spectroscopy of plasma. Dis Aquat Organ 65:107–114

    PubMed  CAS  Google Scholar 

  • Solomon PS, Tan KC, Oliver RP (2005) Mannitol 1-phosphate metabolism is required for sporulation in planta of the wheat pathogen Stagonospora nodorum. Mol Plant Microbe Interact 18:110–115

    PubMed  CAS  Google Scholar 

  • Srinivasan J, Kaplan F, Ajredini R, Zachariah C, Alborn HT, Teal PEA, Malik RU, Edison AS, Sternberg PW, Schroeder FC (2008) A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature 454:1115–U1146

    Google Scholar 

  • Stastny M, Schaffner U, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93:27–37

    Google Scholar 

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

    Google Scholar 

  • Story JM, Storey KB (1983) Regulation of cryoprotectant metabolism in the overwintering gall fly larva, Eurosta-solidaginis––temperature control of glycerol and sorbitol levels. J Comp Physiol 149:495–502

    Google Scholar 

  • Strack D, Ammer C, Schliemann W (2006) Metabolic profiling of arbuscular mycorrhizal roots of Medicago truncatula. In: Ward JL, Beale MH (eds) Proceedings from the 4th international plant metabolomics conference, 276. Metabolomics 2:269–334

    Google Scholar 

  • Sumner LW, Mendes P, Dixon RA (2003) Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochemistry 62:817–836

    PubMed  CAS  Google Scholar 

  • Sun XM, Zhang JX, Zhang HJ, Ni YW, Zhang Q, Chen JP, Guan YF (2010) The responses of Arabidopsis thaliana to cadmium exposure explored via metabolite profiling. Chemosphere 78:840–845

    PubMed  CAS  Google Scholar 

  • Tang HR, Xiao CN, Wang YL (2009) Important roles of the hyphenated HPLC-DAD-MS-SPE-NMR technique in metabonomics. Mag Reson Chem 47:S157–S162

    CAS  Google Scholar 

  • Taylor NS, Weber RJM, Southam AD, Payne TG, Hrydziuszko O, Arvanitis TN, Viant MR (2009) A new approach to toxicity testing in Daphnia magna: application of high throughput FT-ICR mass spectrometry metabolomics. Metabolomics 5:44–58

    CAS  Google Scholar 

  • Trenkamp S, Eckes P, Busch M, Fernie AR (2009) Temporally resolved GC-MS-based metabolic profiling of herbicide treated plants treated reveals that changes in polar primary metabolites alone can distinguish herbicides of differing mode of action. Metabolomics 5:277–291

    PubMed  CAS  Google Scholar 

  • Tucker DJ, Wallis IR, Bolton JM, Marsh KJ, Rosser AA, Brereton IM, Nicolle D, Foley WJ (2010) A metabolomic approach to identifying chemical mediators of mammal-plant interactions. J Chem Ecol 36:727–735

    PubMed  CAS  Google Scholar 

  • Tuffnail W, Mills GA, Cary P, Greenwood R (2009) An environmental H-1 NMR metabolomic study of the exposure of the marine mussel Mytilus edulis to atrazine, lindane, hypoxia and starvation. Metabolomics 5:33–43

    CAS  Google Scholar 

  • Turner MA, Viant MR, Teh SJ, Johnson ML (2007) Developmental rates, structural asymmetry, and metabolic fingerprints of steelhead trout (Oncorhynchus mykiss) eggs incubated at two temperatures. Fish Physio Biochem 33:59–72

    CAS  Google Scholar 

  • Urbanczyk-Wochniak E, Fernie AR (2005) Metabolic profiling reveals altered nitrogen nutrient regimes have diverse effects on the metabolism of hydroponically-grown tomato (Solanum lycopersicum) plants. J Exp Bot 56:309–321

    PubMed  CAS  Google Scholar 

  • van der Meer J (2006) Metabolic theories in ecology. Trends Ecol Evol 21:136–140

    PubMed  Google Scholar 

  • Vasquez-Robinet C, Mane SP, Ulanov AV, Watkinson JI, Stromberg VK, De Koeyer D, Schafleitner R, Willmot DB, Bonierbale M, Bohnert HJ, Grene R (2008) Physiological and molecular adaptations to drought in Andean potato genotypes. J Exp Bot 59:2109–2123

    PubMed  CAS  Google Scholar 

  • Verpoorte R, Choi YH, Mustafa NR, Kim HK (2008) Metabolomics: back to basics. Phytochem Rev 7:525–537

    CAS  Google Scholar 

  • Via S, Gomulkiewicz R, Dejong G, Scheiner SM, Schlichting CD, Vantienderen PH (1995) Adaptive phenotypic plasticity––consensus and controversy. Trends Ecol Evol 10:212–217

    PubMed  CAS  Google Scholar 

  • Viant MR (2007) Metabolomics of aquatic organisms: the new ‘omics’ on the block. Mar Ecol Prog Ser 332:301–306

    CAS  Google Scholar 

  • Viant MR, Werner I, Rosenblum ES, Gantner AS, Tjeerdema RS, Johnson ML (2003) Correlation between heat-shock protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature. Fish Physio Biochem 29:159–171

    CAS  Google Scholar 

  • Viant MR, Pincetich CA, Eerderna RST (2006a) Metabolic effects of dinoseb, diazinon-and esfenvalerate in eyed eggs and alevins of Chinook salmon (Oncorhynchus tshawytscha) determined by H-1 NMR metabolomics. Aquat Toxicol 77:359–371

    PubMed  CAS  Google Scholar 

  • Viant MR, Pincetich CA, Hinton DE, Tjeerdema RS (2006b) Toxic actions of dinoseb in medaka (Oryzias latipes) embryos as determined by in vivo P-31 NMR, HPLC-UV and H-1 NMR metabolomics. Aquat Toxicol 76:329–342

    PubMed  CAS  Google Scholar 

  • Vikram A, Prithiviraj B, Hamzehzarghani H, Kushalappa A (2004) Volatile metabolite profiling to discriminate diseases of McIntosh apple inoculated with fungal pathogens. J Sci Food Agr 84:1333–1340

    CAS  Google Scholar 

  • Waagner D, Heckmann LH, Malmendal A, Nielsen NC, Holmstrup M, Bayley M (2010) Hsp70 expression and metabolite composition in response to short-term thermal changes in Folsomia candida (Collembola). Comp Biochem Phys A 157:177–183

    Google Scholar 

  • Wallenstein MD, Hess AM, Lewis MR, Steltzerae H, Ayres E (2010) Decomposition of aspen leaf litter results in unique metabolomes when decomposed under different tree species. Soil Biol Biochem 42:484–490

    CAS  Google Scholar 

  • Ward JL, Forcat S, Beckmann M, Bennett M, Miller SJ, Baker JM, Hawkins ND, Vermeer CP, Lu CA, Lin WC, Truman WM, Beale MH, Draper J, Mansfield JW, Grant M (2010) The metabolic transition during disease following infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Plant J 63:443–457

    CAS  Google Scholar 

  • Warne MA, Lenz EM, Osborn D, Weeks JM, Nicholson JK (2000) An NMR-based metabonomic investigation of the toxic effects of 3-trifluoromethyl-aniline on the earthworm Eisenia veneta. Biomarkers 5:56–72

    CAS  Google Scholar 

  • Warne MA, Lenz EM, Osborn D, Weeks JM, Nicholson JK (2001) Comparative biochemistry and short-term starvation effects on the earthworms Eisenia veneta and Lumbricus terrestris studied by H-1 NMR spectroscopy and pattern recognition. Soil Biol Biochem 33:1171–1180

    CAS  Google Scholar 

  • Weckwerth W (2008) Integration of metabolomics and proteomics in Mol Plant Physiology––coping with the complexity by data-dimensionality reduction. Physiol Plantarum 132:176–189

    CAS  Google Scholar 

  • West GB, Brown JH, Enquist BJ (1999) The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284:1677–1679

    PubMed  CAS  Google Scholar 

  • 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. J Chem Ecol 32:2417–2428

    PubMed  CAS  Google Scholar 

  • Widodo PattersonJH, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. J Exp Bot 60:4089–4103

    PubMed  CAS  Google Scholar 

  • Wienkoop S, Morgenthal K, Wolschin F, Scholz M, Selbig J, Weckwerth W (2008) Integration of metabolomic and proteomic phenotypes. Mol Cell Proteomics 7:1725–1736

    PubMed  CAS  Google Scholar 

  • Williams TD, Wu HF, Santos EM, Ball J, Katsiadaki I, Brown MM, Baker P, Ortega F, Falciani F, Craft JA, Tyler CR, Chipman JK, Viant MR (2009) Hepatic transcriptomic and metabolomic responses in the stickleback (Gasterosteus aculeatus) exposed to environmentally relevant concentrations of dibenzanthracene. Environ Sci Technol 43:6341–6348

    PubMed  CAS  Google Scholar 

  • Yamakawa H, Hakata M (2010) Atlas of rice grain filling-related metabolism under high temperature: joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation. Plant Cell Physiol 51:795–809

    PubMed  CAS  Google Scholar 

  • Yang WL, Bernards MA (2007) Metabolite profiling of potato (Solanum tuberosum L.) tubers during wound-induced suberization. Metabolomics 3:147–159

    CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Spanish Government project CGL2006-04025/BOS, CGC2010-17172 and Consolider-Ingenio Montes (CSD2008-00040), by the Catalan Government project SGR 2009-458, and by the European project NEU NITROEUROPE GOCE017841.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jordi Sardans.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sardans, J., Peñuelas, J. & Rivas-Ubach, A. Ecological metabolomics: overview of current developments and future challenges. Chemoecology 21, 191–225 (2011). https://doi.org/10.1007/s00049-011-0083-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00049-011-0083-5

Keywords

Navigation