Different "metabolomic niches" of the highly diverse tree species of the French Guiana rainforests

. 2020 Apr 24 ; 10 (1) : 6937. [epub] 20200424

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32332903
Odkazy

PubMed 32332903
PubMed Central PMC7181821
DOI 10.1038/s41598-020-63891-y
PII: 10.1038/s41598-020-63891-y
Knihovny.cz E-zdroje

Tropical rainforests harbor a particularly high plant diversity. We hypothesize that potential causes underlying this high diversity should be linked to distinct overall functionality (defense and growth allocation, anti-stress mechanisms, reproduction) among the different sympatric taxa. In this study we tested the hypothesis of the existence of a metabolomic niche related to a species-specific differential use and allocation of metabolites. We tested this hypothesis by comparing leaf metabolomic profiles of 54 species in two rainforests of French Guiana. Species identity explained most of the variation in the metabolome, with a species-specific metabolomic profile across dry and wet seasons. In addition to this "homeostatic" species-specific metabolomic profile significantly linked to phylogenetic distances, also part of the variance (flexibility) of the metabolomic profile was explained by season within a single species. Our results support the hypothesis of the high diversity in tropical forest being related to a species-specific metabolomic niche and highlight ecometabolomics as a tool to identify this species functional diversity related and consistent with the ecological niche theory.

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Connell JH. Diversity in tropical rain forests and coral reefs. Science (80-.). 1978;199:1302–1310. doi: 10.1126/science.199.4335.1302. PubMed DOI

John R, et al. Soil nutrients influence spatial distributions of tropical tree species. Proc. Natl. Acad. Sci. USA. 2007;104:864–9. doi: 10.1073/pnas.0604666104. PubMed DOI PMC

Wright SJ. Plant diversity in tropical forests: A review of mechanisms of species coexistence. Oecologia. 2002;130:1–14. doi: 10.1007/s004420100809. PubMed DOI

Volkov I, Banavar JR, He FL, Hubbell SP, Maritan A. Density dependence explains tree species abundance and diversity in tropical forests. Nature. 2005;438:658–661. doi: 10.1038/nature04030. PubMed DOI

Aiba SI, et al. Structure, floristics and diversity of tropical montane rain forests over ultramafic soils on Mount Kinabalu (Borneo) compared with those on non-ultramafic soils. Aust. J. Bot. 2015;63:191–203. doi: 10.1071/BT14238. DOI

Martins KG, Marques MCM, dos Santos E, Marques R. Effects of soil conditions on the diversity of tropical forests across a successional gradient. For. Ecol. Manage. 2015;349:4–11. doi: 10.1016/j.foreco.2015.04.018. DOI

LeBauer DS, Treseder KK. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology. 2008;89:371–9. doi: 10.1890/06-2057.1. PubMed DOI

Fujii K, et al. Plant–soil interactions maintain biodiversity and functions of tropical forest ecosystems. Ecol. Res. 2017;33:1–12.

Xu W, et al. Soil phosphorus heterogeneity promotes tree species diversity and phylogenetic clustering in a tropical seasonal rainforest. Ecol. Evol. 2016;6:8719–8726. doi: 10.1002/ece3.2529. PubMed DOI PMC

Pennington RT, Lavin M, Oliveira-Filho A. Woody Plant Diversity, Evolution, and Ecology in the Tropics: Perspectives from Seasonally Dry Tropical Forests. Annu. Rev. Ecol. Evol. Syst. 2009;40:437–457. doi: 10.1146/annurev.ecolsys.110308.120327. DOI

Matos FAR, et al. Effects of landscape configuration and composition on phylogenetic diversity of trees in a highly fragmented tropical forest. J. Ecol. 2017;105:265–276. doi: 10.1111/1365-2745.12661. DOI

Clark, D. B., Clark, D. A. & Read, J. M. Edaphic variation and the mesoscale distribution of tree species in a neotropical rain forest. J. Ecol. 101–112 (1998).

Mandl NA, Kessler M, Robbert Gradstein S. Effects of environmental heterogeneity on species diversity and composition of terrestrial bryophyte assemblages in tropical montane forests of southern Ecuador. Plant Ecol. Divers. 2009;2:313–321. doi: 10.1080/17550870903341877. DOI

Becerra JX. On the factors that promote the diversity of herbivorous insects and plants in tropical forests. Proc. Natl. Acad. Sci. 2015;112:6098–6103. doi: 10.1073/pnas.1418643112. PubMed DOI PMC

Hutchinson G. Concluding remarks. Cold Spring Harb Symp Quant Biol. 1957;22:415–427. doi: 10.1101/SQB.1957.022.01.039. DOI

Mouillot D, et al. Niche overlap estimates based on quantitative functional traits: A new family of non-parametric indices. Oecologia. 2005;145:345–353. doi: 10.1007/s00442-005-0151-z. PubMed DOI

Kraft NJB, Valencia R, Ackerly DD. Functional Traits and Niche-Based Tree Community Assembly in an Amazonian. Forest. Science (80-.). 2008;322:580–582. doi: 10.1126/science.1160662. PubMed DOI

Kraft NJ, Godoy O, Levine JM. Plant functional traits and the multidimensional nature of species coexistence. Proc. Natl. Acad. Sci. 2015;112:797–802. doi: 10.1073/pnas.1413650112. PubMed DOI PMC

Baraloto C, et al. Using functional traits and phylogenetic trees to examine the assembly of tropical tree communities. J. Ecol. 2012;100:690–701. doi: 10.1111/j.1365-2745.2012.01966.x. DOI

Gargallo-Garriga A, et al. Long-term fertilization determines different metabolomic profiles and responses in saplings of three rainforest tree species with different adult canopy position. PLoS One. 2017;12:1–21. doi: 10.1371/journal.pone.0177030. PubMed DOI PMC

Gargallo-Garriga A, et al. Impact of Soil Warming on the Plant Metabolome of Icelandic Grasslands. Metabolites. 2017;7:44. doi: 10.3390/metabo7030044. PubMed DOI PMC

Macel M, van dam NM, Keurentjes JJB. Metabolomics: The chemistry between ecology and genetics. Mol. Ecol. Resour. 2010;10:583–593. doi: 10.1111/j.1755-0998.2010.02854.x. PubMed DOI

Lee S, et al. Exploring the metabolomic diversity of plant species across spatial (leaf and stem) components and phylogenic groups. BMC Plant Biol. 2020;20:1–10. doi: 10.1186/s12870-019-2231-y. PubMed DOI PMC

Loskutov IG, et al. Application of Metabolomic Analysis in Exploration of Plant Genetic Resources. Proc. Latv. Acad. Sci. Sect. B. Nat. Exact, Appl. Sci. 2019;73:494–501.

Peñuelas, J. et al. The bioelements, the elementome and the “biogeochemical niche”. Under Revis. Nat. Ecol. Evol. (2018).

Fiehn O, et al. Metabolite profiling for plant functional genomics. Nat. Biotechnol. 2000;18:1157–61. doi: 10.1038/81137. PubMed DOI

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

Leiss KA, Choi YH, Verpoorte R, Klinkhamer PGL. An overview of NMR-based metabolomics to identify secondary plant compounds involved in host plant resistance. Phytochem. Rev. 2011;10:205–216. doi: 10.1007/s11101-010-9175-z. PubMed DOI PMC

Gargallo-Garriga A, et al. Opposite metabolic responses of shoots and roots to drought. Sci. Rep. 2014;4:6829. doi: 10.1038/srep06829. PubMed DOI PMC

Peñuelas J, Sardans J. Ecology: Elementary factors. Nature. 2009;460:803–804. doi: 10.1038/460803a. PubMed DOI

Fiehn O. Metabolomics–the link between genotypes and phenotypes. Plant Mol. Biol. 2002;48:155–71. doi: 10.1023/A:1013713905833. PubMed DOI

Weckwerth W, Loureiro ME, Wenzel K, Fiehn O. Differential metabolic networks unravel the effects of silent plant phenotypes. Proc. Natl. Acad. Sci. USA. 2004;101:7809–14. doi: 10.1073/pnas.0303415101. PubMed DOI PMC

Gargallo-Garriga A, et al. Warming differentially influences the effects of drought on stoichiometry and metabolomics in shoots and roots. New Phytol. 2015;207:591–603. doi: 10.1111/nph.13377. PubMed DOI

Sardans, J. et al. Metabolic responses of Quercus ilex seedlings to wounding analysed with nuclear magnetic resonance profiling. Plant Biol. 16 (2014). PubMed

Gargallo-Garriga, A. et al. Shifts in plant foliar and floral metabolomes in response to the suppression of the associated microbiota. BMC Plant Biol. 16 (2016). PubMed PMC

Scherling C, Roscher C, Giavalisco P, Schulze ED, Weckwerth W. Metabolomics unravel contrasting effects of biodiversity on the performance of individual plant species. PLoS One. 2010;5:1–13. doi: 10.1371/journal.pone.0012569. PubMed DOI PMC

Williams WT, Lance GN, Webb LJ, Tracey JG, Connell JH. Studies in the Numerical Analysis of Complex Rain-Forest Communities: IV. A Method for the Elucidation of Small-Scale Forest Pattern. J. Ecol. 1969;57:635–654. doi: 10.2307/2258489. DOI

Whitmore, T. C. Tropical Rain Forests of the Far East. (1975).

Richards, P. W. The tropical rain forest; an ecological study. (1952).

Janzen DH. Herbivores and the number of tree species in tropical forests. Am. Nat. 1970;104:501–528. doi: 10.1086/282687. DOI

Macel M, et al. Novel chemistry of invasive plants: exotic species have more unique metabolomic profiles than native congeners. Ecol. Evol. 2014;4:2777–2786. doi: 10.1002/ece3.1132. PubMed DOI PMC

Peñuelas J, et al. Faster returns on ‘leaf economics’ and different biogeochemical niche in invasive compared with native plant species. Glob. Chang. Biol. 2009;16:2171–2185. doi: 10.1111/j.1365-2486.2009.02054.x. DOI

Peñuelas J, Sardans J, Ogaya R, Estiarte M. Nutrient stoichiometric relations and biogeochemical niche in coexisting plant species: Effect of simulated climate change. Polish J. Ecol. 2008;56:613–622.

Sardans J, et al. Foliar elemental composition of European forest tree species associated with evolutionary traits and present environmental and competitive conditions. Glob. Ecol. Biogeogr. 2015;24:240–255. doi: 10.1111/geb.12253. DOI

Sardans J, Peñuelas J. Tree growth changes with climate and forest type are associated with relative allocation of nutrients, especially phosphorus, to leaves and wood. Glob. Ecol. Biogeogr. 2013;22:494–507. doi: 10.1111/geb.12015. DOI

Sardans J, Peñuelas J. Hydraulic redistribution by plants and nutrient stoichiometry: Shifts under global change. Ecohydrology. 2014;7:1–20. doi: 10.1002/eco.1459. DOI

Urbina I, et al. Shifts in the elemental composition of plants during a very severe drought. Environ. Exp. Bot. 2015;111:63–73. doi: 10.1016/j.envexpbot.2014.10.005. PubMed DOI PMC

Yu Q, et al. Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecol. Lett. 2010;13:1390–1399. doi: 10.1111/j.1461-0248.2010.01532.x. PubMed DOI

Ricklefs RE. Environmental heterogeneity and plant species diversity: a hypothesis. Am. Nat. 1977;111:376–381. doi: 10.1086/283169. DOI

Zas R, Fernández-López J. Juvenile genetic parameters and genotypic stability of Pinus pinaster Ait. open-pollinated families under different water and nutrient regimes. For. Sci. 2005;51:165–174.

Martens S, Mithöfer A. Flavones and flavone synthases. Phytochemistry. 2005;66:2399–2407. doi: 10.1016/j.phytochem.2005.07.013. PubMed DOI

Bravo, L. Polyphenols: Chemistry, dietary sources, metabolism, and nutritional signifi… Nutr. Rev. 56 (1998). PubMed

Klem K, et al. Ultraviolet and photosynthetically active radiation can both induce photoprotective capacity allowing barley to overcome high radiation stress. Plant Physiol. Biochem. 2015;93:74–83. doi: 10.1016/j.plaphy.2015.01.001. PubMed DOI

Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM. The Role of Root Exudates in Rhizosphere Interactions With Plants and Other Organisms. Annu. Rev. Plant Biol. 2006;57:233–266. doi: 10.1146/annurev.arplant.57.032905.105159. PubMed DOI

Dam NMV, Bouwmeester HJ. Metabolomics in the Rhizosphere: Tapping into Belowground Chemical Communication. Trends Plant Sci. 2016;xx:1–10. PubMed

Nakabayashi R, et al. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 2014;77:367–379. doi: 10.1111/tpj.12388. PubMed DOI PMC

Meijón M, et al. Exploring natural variation of Pinus pinaster Aiton using metabolomics: Is it possible to identify the region of origin of a pine from its metabolites? Mol. Ecol. 2016;25:959–976. doi: 10.1111/mec.13525. PubMed DOI

Chapin FS, Shaver GR, Giblin AE, Nadelhoffer KJ, Laundre JA. Responses of Arctic Tundra to Experimental and Observed Changes in Climate RESPONSES OF ARCTIC TUNDRA TO EXPERIMENTAL AND OBSERVED. CHANGES IN CLIMATE’. 1995;76:694–711.

Marino G, Aqil M, Shipley B. The leaf economics spectrum and the prediction of photosynthetic light-response curves. Funct. Ecol. 2010;24:263–272. doi: 10.1111/j.1365-2435.2009.01630.x. DOI

Estiarte M, Peñuelas J. Excess carbon: the relationship with phenotypical plasticity in storage and defense functions of plants. Orsis Org. i Sist. Rev. botànica Zool. i Ecol. 1999;14:159–203.

Zhao HJ, Zou Q. Protective effects of exogenous antioxidants and phenolic compounds on photosynthesis of wheat leaves under high irradiance and oxidative stress. Photosynthetica. 2002;40:523–527. doi: 10.1023/A:1024339716382. DOI

Martz F, Jaakola L, Julkunen-Tiitto R, Stark S. Phenolic Composition and Antioxidant Capacity of Bilberry (Vaccinium myrtillus) Leaves in Northern Europe Following Foliar Development and Along Environmental Gradients. J. Chem. Ecol. 2010;36:1017–1028. doi: 10.1007/s10886-010-9836-9. PubMed DOI

Lim, T. Y., Lim, Y. Y. & Yule, C. M. Distribution and characterisation of phenolic compounds in Macaranga pruinosa and associated soils in a tropical peat swamp forest. J. Trop. For. Sci. 509–518 (2017).

Sipura M, Ikonen A, Tahvanainen J, Roininen H. Why does the leaf beetle Galerucella lineola F. Attack wetland willows? Ecology. 2002;83:3393–3407. doi: 10.1890/0012-9658(2002)083[3393:WDTLBG]2.0.CO;2. DOI

Khang DT, et al. Involvement of Phenolic Compounds in Anaerobic Flooding Germination of Rice (Oryza sativa L.) Int. Lett. Nat. Sci. 2016;56:73–81.

Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA. Strigolactone Acts Downstream of Auxin to Regulate Bud Outgrowth in Pea and Arabidopsis. Plant Physiol. 2009;150:482–493. doi: 10.1104/pp.108.134783. PubMed DOI PMC

Me Chave JR, Ra BR, Dubois M-A. Estimation of biomass in a neotropical forest of French Guiana: spatial and temporal variability. J. Trop. Ecol. 2001;17:79–96. doi: 10.1017/S0266467401001055. DOI

Gourlet-Fleury, S., Guehl, J.-M. & Laroussinie, O. Ecology and management of a neotropical rainforest: lessons drawn from Paracou, a long-term experimental research site in French Guiana. Elseiver (2004).

Courtois, E. A. et al. Spatial Variation of Soil CO2, CH4 and N2O Fluxes Across Topographical Positions in Tropical Forests of the Guiana Shield. Ecosystems, 10.1007/s10021-018-0232-6 (2018).

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

Rivas-Ubach, A. et al. Ecometabolomics: Optimized NMR-based method. Methods Ecol. Evol. 4 (2013).

Deborde C, et al. Plant metabolism as studied by NMR spectroscopy. Prog. Nucl. Magn. Reson. Spectrosc. 2017;102–103:61–97. doi: 10.1016/j.pnmrs.2017.05.001. PubMed DOI

Wilson ID, et al. HPLC-MS-based methods for the study of metabonomics. J. Chromatogr. B. 2005;817:67–76. doi: 10.1016/j.jchromb.2004.07.045. PubMed DOI

Ogata H, et al. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 1999;27:29–34. doi: 10.1093/nar/27.1.29. PubMed DOI PMC

Neumann S, Böcker S. Computational mass spectrometry for metabolomics: Identification of metabolites and small molecules. Anal. Bioanal. Chem. 2010;398:2779–2788. doi: 10.1007/s00216-010-4142-5. PubMed DOI

Smith CA, Want EJ, O’maille G, Abagyan R, Siuzdak G. XCMS: Processing Mass Spectrometry Data for Metabolite Profiling Using Nonlinear Peak Alignment, Matching, and Identification. Anal. Chem. 2006;78:779–787. doi: 10.1021/ac051437y. PubMed DOI

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