Leaf metabolic traits reveal hidden dimensions of plant form and function

Tom W.N. Walker; Franziska Schrodt; Pierre Marie Allard; Emmanuel Defossez; Vincent E.J. Jassey; Meredith C. Schuman; Jake M. Alexander; Oliver Baines; Virginie Baldy; Richard D. Bardgett; Pol Capdevila; Phyllis D. Coley; Nicole M. van Dam; Bruno David; Patrice Descombes; María José Endara; Catherine Fernandez; Dale Forrister; Albert Gargallo-Garriga; Gaëtan Glauser; Sue Marr; Steffen Neumann; Loïc Pellissier; Kristian Peters; Sergio Rasmann; Ute Roessner; Roberto Salguero-Gómez; Jordi Sardans; Wolfram Weckwerth; Jean Luc Wolfender; Josep Peñuelas

doi:10.1126/sciadv.adi4029

Leaf metabolic traits reveal hidden dimensions of plant form and function

Tom W.N. Walker
, Franziska Schrodt
, Pierre Marie Allard
, Emmanuel Defossez
, Vincent E.J. Jassey
, Meredith C. Schuman
, Jake M. Alexander
, Oliver Baines
, Virginie Baldy
, Richard D. Bardgett
, Pol Capdevila
, Phyllis D. Coley
, Nicole M. van Dam
, Bruno David
, Patrice Descombes
, María José Endara
, Catherine Fernandez
, Dale Forrister
, Albert Gargallo-Garriga
, Gaëtan Glauser

Sue Marr, Steffen Neumann, Loïc Pellissier, Kristian Peters, Sergio Rasmann, Ute Roessner, Roberto Salguero-Gómez, Jordi Sardans, Wolfram Weckwerth, Jean Luc Wolfender, Josep Peñuelas

Functional and Evolutionary Ecology

Publications: Contribution to journal › Article › Peer Reviewed

Abstract

The metabolome is the biochemical basis of plant form and function, but we know little about its macroecological variation across the plant kingdom. Here, we used the plant functional trait concept to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five metabolic functional traits reveals that plants vary on two major axes of leaf metabolic specialization—a leaf chemical defense spectrum and an expression of leaf longevity. Axes are similar for tropical and temperate species, with many trait combinations being viable. However, metabolic traits vary orthogonally to life-history strategies described by widely used functional traits. The metabolome thus expands the functional trait concept by providing additional axes of metabolic specialization for examining plant form and function.

Original language	English
Article number	eadi4029
Journal	Science Advances
Volume	9
Issue number	35
DOIs	https://doi.org/10.1126/sciadv.adi4029
Publication status	Published - 2023

Funding

We thank J. Clément and G. Vieilledent for building bespoke functionality into the R package “jSDM” for exploratory analyses. Funding: This study was partly funded by a grant from the Synthesis Centre (sDiv) of the German Centre for Integrative Biodiversity Research (iDiv), awarded to T.W.N.W., F.S., and N.M.v.D. Plant material collection and metabolomics analysis were financed by Swiss National Science Foundation grants awarded to L.P. (grant no. 31003A-162604), S.R. (grant no. 31003A-131956), and J.-L.W. (grant no. CRSII5-189921/1). J.M.A. and T.W.N.W. were funded by a Swiss National Science Foundation grant (grant no. 31003A-176044). F.S. acknowledges funding by the University of Nottingham Anne McLaren Fellowship. E.D., T.W.N.W., and S.R. are funded by a Swiss National Science Foundation grant (grant no. 31003A_179481) awarded to S.R. V.E.J.J. is funded by the French National Research Agency (grant no. ANR-17-CE01-0007: Mixxopeat). V.B. is supported by the French Agence Nationale pour la Recherche (grant no. ANR-12-BSV7-0016-01: SecPriMe2), the BioDivMeX Mistrals program, the Aix-Marseille University ‘Investissements d’Avenir’ program, and the Labex OT-Med programs. P.C. is supported by a Ramón Areces Foundation Postdoctoral Scholarship. P.D.C .is funded by the U.S. National Science Foundation (grant no. DEB-1135733). N.M.v.D., S.M., and K.P. are supported by iDiv Halle-Jena-Leipzig, which is funded by the German Research Foundation (grant nos DFG–FZT 118, 202548816). S.N. and K.P. are additionally funded by the German Network for Bioinformatics Infrastructure (de.NBI) and acknowledge BMBF funding (grant no. 031 L0107). D.L.F. is supported by the U.S. National Science Foundation Graduate Research Fellowships Program. R.S.-G. is funded by a U.K. Natural Environment Research Council Independent Research Fellowship (grant no. NE/M018458/1). J.P. and J.S. are funded by the Spanish Government (grant no. CGL2016-79835), Catalan Government (grant no. SGR 2017-1005), and a European Research Council Synergy Grant (grant no. ERC-SyG-2013-610028: IMBALANCE-P). M.C.S. is supported by a NOMIS Foundation project (“Remotely Sensing Ecological Genomics”) and by the University of Zürich Research Priority Program on Global Change and Biodiversity. J.-L.W. and P.M.A. are funded by a Swiss National Science Foundation grant (grant no. CRSII5_189921/1). Acknowledgments:W ethankJ.ClémentandG.Vieilledentforbuildingbespokefunctionality intotheRpackage“jSDM”forexplora tory analyses.Funding:Thisstudywaspartlyfundedbya grantfromtheSynthesisCentr e(sDiv)oftheGermanCentr eforIntegrativeBiodiversity Research(iDiv),awardedtoT .W .N.W ., F .S., andN.M.v.D.Plantmaterialcollectionand metabolomicsanalysiswerefinancedbySwissNationalScienceFoundationgrantsawardedto L.P .(grantno.31003A-162604),S.R.(grantno.31003A-131956),andJ.-L.W .(grantno.CRSII5-189921/1).J.M.A.andT .W .N.W .werefundedbyaSwissNationalScienceFoundationgrant (grantno.31003A-176044).F .S. acknowledgesfundingbytheUniversityofNottinghamAnne McLarenFellowship.E.D.,T .W .N.W ., andS.R.arefundedbyaSwissNationalScienceFoundation grant(grantno.31003A_179481)awardedtoS.R.V .E.J.J. isfundedbytheFrenchNational ResearchAgency(grantno.ANR-17-CE01-0007:Mixxopeat).V .B. issupportedbytheFrench AgenceNationalepourlaRecherche(grantno.ANR-12-BSV7-0016-01:SecPriMe2),the BioDivMeX Mistrals progr am, the Aix-Marseille University ‘Investissements d’A venir’ program, andtheLabexOT-Medprogr ams. P .C. issupportedbyaRamónArecesFoundationPos tdoctor al Scholarship.P .D.C .isfundedbytheU.S.NationalScienceFoundation(grantno.DEB-1135733). N.M.v.D.,S.M.,andK.P .aresupportedbyiDivHalle-Jena-Leipzig,whichisfundedbytheGerman ResearchFoundation(grantnosDFG–FZT118,202548816).S.N.andK.P .areadditionallyfunded bytheGermanNetworkforBioinformaticsInfrastructure(de.NBI)andacknowledgeBMBF funding(grantno.031L0107).D.L.F .issupportedbytheU.S.NationalScienceFoundation GraduateResearchFellowshipsProgram.R.S.-G.isfundedbyaU.K.NaturalEnvironment ResearchCouncilIndependentResearchFellowship(grantno.NE/M018458/1).J.P .andJ.S.are fundedbytheSpanishGovernment(grantno.CGL2016-79835),CatalanGovernment(grantno. SGR2017-1005),andaEuropeanResearchCouncilSynergyGrant(grantno.ERC-SyG-2013- 610028:IMBALANCE-P).M.C.S.issupportedbyaNOMISFoundationproject(“RemotelySensing EcologicalGenomics”)andbytheUniversityofZürichResearchPriorityProgramonGlobal ChangeandBiodiversity.J.-L.W .andP .M.A. arefundedbyaSwissNationalScienceFoundation grant(grantno.CRSII5_189921/1).Authorcontributions:Conceptualization:T .W .N.W .in collaborationwithP .-M.A., R.D.B.,P .C., B.D.,E.D.,A.G.-G.,V .E.J.J., J.P ., S.R.,R.S.-G.,J.S.,M.C.S.,F .S., N.M.v.D.,andW .W ., withsupportfromallco-authors.Fundingacquisition:F .S., .N.M.v.D.,and T .W .N.W .Datacollection:P .-M.A., E.D.,andB.D.Datacuration:T .W .N.W ., withsupportfromP .-M.A.,O.B.,P .C., andE.D.Formalanalysis:T .W .N.W ., withsupportfromP .C., E.D.,M.-J.E.,.D.F ,and V .E.J.J. Writing:T .W .N.W ., withsupportfromM.C.S.Reviewingandediting:Allco-authors. Competinginterests:Theauthorsdeclarethattheyhav enocompetinginterests.Dataand materialsavailability:RawtropicalmetabolomicsdataareavailableundertheDOI10.25345/ C59J97 (36). Raw temperate species metabolomics data are available on GNPS using the link https://gnps.ucsd.edu/ProteoSAFe/status.jsp?task=32bb23eb0e0b475da0336f6f84254d05 (37). Flat data and R code are available under the DOI 10.5061/dryad.zpc866tdn. W orking data analysisfolderstructureisdownloadableundertheDOI10.17605/OSF .IO/YZR4C. Alldata neededtoevaluatetheconclusionsinthepaperarepresentinthepaperand/orthe SupplementaryMaterials.

Austrian Fields of Science 2012

106057 Metabolomics
106044 Systems biology

Keywords

metabolomics
metabolome
plant chemistry
functional traits

Access to Document

10.1126/sciadv.adi4029

https://phaidra.univie.ac.at/o:2068102Licence: CC BY 4.0

Cite this

Walker, T. W. N., Schrodt, F., Allard, P. M., Defossez, E., Jassey, V. E. J., Schuman, M. C., Alexander, J. M., Baines, O., Baldy, V., Bardgett, R. D., Capdevila, P., Coley, P. D., van Dam, N. M., David, B., Descombes, P., Endara, M. J., Fernandez, C., Forrister, D., Gargallo-Garriga, A., ... Peñuelas, J. (2023). Leaf metabolic traits reveal hidden dimensions of plant form and function. Science Advances, 9(35), Article eadi4029. https://doi.org/10.1126/sciadv.adi4029

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title = "Leaf metabolic traits reveal hidden dimensions of plant form and function",

abstract = "The metabolome is the biochemical basis of plant form and function, but we know little about its macroecological variation across the plant kingdom. Here, we used the plant functional trait concept to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five metabolic functional traits reveals that plants vary on two major axes of leaf metabolic specialization{\textemdash}a leaf chemical defense spectrum and an expression of leaf longevity. Axes are similar for tropical and temperate species, with many trait combinations being viable. However, metabolic traits vary orthogonally to life-history strategies described by widely used functional traits. The metabolome thus expands the functional trait concept by providing additional axes of metabolic specialization for examining plant form and function.",

keywords = "metabolomics, metabolome, plant chemistry, functional traits",

author = "Walker, \{Tom W.N.\} and Franziska Schrodt and Allard, \{Pierre Marie\} and Emmanuel Defossez and Jassey, \{Vincent E.J.\} and Schuman, \{Meredith C.\} and Alexander, \{Jake M.\} and Oliver Baines and Virginie Baldy and Bardgett, \{Richard D.\} and Pol Capdevila and Coley, \{Phyllis D.\} and \{van Dam\}, \{Nicole M.\} and Bruno David and Patrice Descombes and Endara, \{Mar{\'i}a Jos{\'e}\} and Catherine Fernandez and Dale Forrister and Albert Gargallo-Garriga and Ga{\"e}tan Glauser and Sue Marr and Steffen Neumann and Lo{\"i}c Pellissier and Kristian Peters and Sergio Rasmann and Ute Roessner and Roberto Salguero-G{\'o}mez and Jordi Sardans and Wolfram Weckwerth and Wolfender, \{Jean Luc\} and Josep Pe{\~n}uelas",

note = "Publisher Copyright: Copyright {\textcopyright} 2023 The Authors,",

year = "2023",

doi = "10.1126/sciadv.adi4029",

language = "English",

volume = "9",

journal = "Science Advances",

issn = "2375-2548",

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Walker, TWN, Schrodt, F, Allard, PM, Defossez, E, Jassey, VEJ, Schuman, MC, Alexander, JM, Baines, O, Baldy, V, Bardgett, RD, Capdevila, P, Coley, PD, van Dam, NM, David, B, Descombes, P, Endara, MJ, Fernandez, C, Forrister, D, Gargallo-Garriga, A, Glauser, G, Marr, S, Neumann, S, Pellissier, L, Peters, K, Rasmann, S, Roessner, U, Salguero-Gómez, R, Sardans, J, Weckwerth, W, Wolfender, JL & Peñuelas, J 2023, 'Leaf metabolic traits reveal hidden dimensions of plant form and function', Science Advances, vol. 9, no. 35, eadi4029. https://doi.org/10.1126/sciadv.adi4029

TY - JOUR

T1 - Leaf metabolic traits reveal hidden dimensions of plant form and function

AU - Walker, Tom W.N.

AU - Schrodt, Franziska

AU - Allard, Pierre Marie

AU - Defossez, Emmanuel

AU - Jassey, Vincent E.J.

AU - Schuman, Meredith C.

AU - Alexander, Jake M.

AU - Baines, Oliver

AU - Baldy, Virginie

AU - Bardgett, Richard D.

AU - Capdevila, Pol

AU - Coley, Phyllis D.

AU - van Dam, Nicole M.

AU - David, Bruno

AU - Descombes, Patrice

AU - Endara, María José

AU - Fernandez, Catherine

AU - Forrister, Dale

AU - Gargallo-Garriga, Albert

AU - Glauser, Gaëtan

AU - Marr, Sue

AU - Neumann, Steffen

AU - Pellissier, Loïc

AU - Peters, Kristian

AU - Rasmann, Sergio

AU - Roessner, Ute

AU - Salguero-Gómez, Roberto

AU - Sardans, Jordi

AU - Weckwerth, Wolfram

AU - Wolfender, Jean Luc

AU - Peñuelas, Josep

PY - 2023

Y1 - 2023

N2 - The metabolome is the biochemical basis of plant form and function, but we know little about its macroecological variation across the plant kingdom. Here, we used the plant functional trait concept to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five metabolic functional traits reveals that plants vary on two major axes of leaf metabolic specialization—a leaf chemical defense spectrum and an expression of leaf longevity. Axes are similar for tropical and temperate species, with many trait combinations being viable. However, metabolic traits vary orthogonally to life-history strategies described by widely used functional traits. The metabolome thus expands the functional trait concept by providing additional axes of metabolic specialization for examining plant form and function.

AB - The metabolome is the biochemical basis of plant form and function, but we know little about its macroecological variation across the plant kingdom. Here, we used the plant functional trait concept to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five metabolic functional traits reveals that plants vary on two major axes of leaf metabolic specialization—a leaf chemical defense spectrum and an expression of leaf longevity. Axes are similar for tropical and temperate species, with many trait combinations being viable. However, metabolic traits vary orthogonally to life-history strategies described by widely used functional traits. The metabolome thus expands the functional trait concept by providing additional axes of metabolic specialization for examining plant form and function.

KW - metabolomics

KW - metabolome

KW - plant chemistry

KW - functional traits

UR - https://www.scopus.com/pages/publications/85169230774

U2 - 10.1126/sciadv.adi4029

DO - 10.1126/sciadv.adi4029

M3 - Article

C2 - 37647404

AN - SCOPUS:85169230774

SN - 2375-2548

VL - 9

JO - Science Advances

JF - Science Advances

IS - 35

M1 - eadi4029

ER -

Leaf metabolic traits reveal hidden dimensions of plant form and function

Abstract

Funding

Austrian Fields of Science 2012

Keywords

Access to Document

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