31P-NMR Metabolomics Revealed Species-Specific Use of Phosphorous in Trees of a French Guiana Rainforest

. 2020 Aug 31 ; 25 (17) : . [epub] 20200831

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32877991

Grantová podpora
Synergy grant ERC-2013-SyG-610028 IMBALANCE-P Synergy grant

Productivity of tropical lowland moist forests is often limited by availability and functional allocation of phosphorus (P) that drives competition among tree species and becomes a key factor in determining forestall community diversity. We used non-target 31P-NMR metabolic profiling to study the foliar P-metabolism of trees of a French Guiana rainforest. The objective was to test the hypotheses that P-use is species-specific, and that species diversity relates to species P-use and concentrations of P-containing compounds, including inorganic phosphates, orthophosphate monoesters and diesters, phosphonates and organic polyphosphates. We found that tree species explained the 59% of variance in 31P-NMR metabolite profiling of leaves. A principal component analysis showed that tree species were separated along PC 1 and PC 2 of detected P-containing compounds, which represented a continuum going from high concentrations of metabolites related to non-active P and P-storage, low total P concentrations and high N:P ratios, to high concentrations of P-containing metabolites related to energy and anabolic metabolism, high total P concentrations and low N:P ratios. These results highlight the species-specific use of P and the existence of species-specific P-use niches that are driven by the distinct species-specific position in a continuum in the P-allocation from P-storage compounds to P-containing molecules related to energy and anabolic metabolism.

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Vos J., Biemond H. Effects of nitrogen on the development and growth of the potato plant. 1. Leaf appearance, expansion growth, life spans of leaves and stem branching. Ann. Bot. 1992;70:27–35. doi: 10.1093/oxfordjournals.aob.a088435. DOI

Evans J.R. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia. 1989;78:9–19. doi: 10.1007/BF00377192. PubMed DOI

Elser J.J., Bracken M.E.S., Cleland E.E., Gruner D.S., Harpole W.S., Hillebrand H., Ngai J.T., Seabloom E.W., Shurin J.B., Smith J.E. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 2007;10:1135–1142. doi: 10.1111/j.1461-0248.2007.01113.x. PubMed DOI

Tanner E.V.J., Vitousek P.M., Cuevas E. experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology. 1998;79:10–22. doi: 10.1890/0012-9658(1998)079[0010:EIONLO]2.0.CO;2. DOI

Walker T.W., Syers J.K. The fate of phosphorus during pedogenesis. Geoderma. 1976;15:1–19. doi: 10.1016/0016-7061(76)90066-5. DOI

Allison S.D., Vitousek P.M. Rapid nutrient cycling in leaf litter from invasive plants in Hawai. Oecologia. 2004;141:612–619. doi: 10.1007/s00442-004-1679-z. PubMed DOI

Wardle D.A., Walker L.R., Bardgett R.D. Ecosystem properties and forest decline in contrasting long-term. Science. 2004;305:509–514. doi: 10.1126/science.1098778. PubMed DOI

Kichenin E., Wardle D.A., Peltzer D.A., Morse C.W., Freschet G.T. Contrasting effects of plant inter- and intraspecific variation on community-level trait measures along an environmental gradient. Funct. Ecol. 2013;27:1254–1261. doi: 10.1111/1365-2435.12116. DOI

Turner B.L., Brenes-Arguedas T., Condit R. Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature. 2018;555:367–370. doi: 10.1038/nature25789. PubMed DOI

Vitousek P.M., Sanford R.L., Jr. Nutrient cycling in moist tropical forest. Ann. Rev. Ecol. Syst. 1986;17:137–167. doi: 10.1146/annurev.es.17.110186.001033. DOI

Vitousek P.M. Nutrient Cycling and Limitation: Hawai‘i as a Model System. Princeton University Press; Princeton, NJ, USA: 2004.

Corlett R.T., Primack R.B. Tropical rainforests and the need for cross-continental comparisons. Trends Ecol. Evol. 2006;21:105–107. doi: 10.1016/j.tree.2005.12.002. PubMed DOI

Aiba S.I., Sawada Y., Takyu M., Eino T., Kitayama K., Repin R. 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

John R., Dalling J.W., Harms K.E., Yavitt J.B., Stallard R.F., Mirabello M., Hubbell S.P., Valencia R., Navarrete H., Vallejo M., et al. Soil nutrients influence spatial distributions of tropical tree species. Proc. Natl. Acad. Sci. USA. 2007;104:864–869. doi: 10.1073/pnas.0604666104. PubMed DOI PMC

Pennington R.T., 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 F.A.R., Magnago L.F.S., Gastauer M., Carreiras J.M.B., Simonelli M., Meira-Neto J.A.A., Edwards D.P. 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

LeBauer D.S., Treseder K.K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology. 2008;89:371–379. doi: 10.1890/06-2057.1. PubMed DOI

Fujii K., Shibata M., Kitajima K., Ichie T., Kitayama K., Turner B.L. Plant–soil interactions maintain biodiversity and functions of tropical forest ecosystems. Ecol. Res. 2017;33:1–12. doi: 10.1007/s11284-017-1511-y. DOI

Xu W., Ci X., Song C., He T., Zhang W., Li Q., Li J. 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

Martins K.G., Marques M.C.M., 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

Mandl N.A., 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

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. 1998;86:101–112. doi: 10.1046/j.1365-2745.1998.00238.x. DOI

Connell J.H. Diversity in tropical rain forests and coral reefs. Science. 1978;199:1302–1310. doi: 10.1126/science.199.4335.1302. PubMed DOI

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

Hidaka A., Kitayama K. Allocation of foliar phosphorus fractions and leaf traits of tropical tree species in response to decreased soil phosphorus availability on Mount Kinabalu, Borneo. J. Ecol. 2011;99:849–857. doi: 10.1111/j.1365-2745.2011.01805.x. DOI

Lambers H., Finnegan P.M., Laliberté E., Pearse S.J., Ryan M.H., Shane M.W., Veneklaas E.J. Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: Are there lessons to be learned for future crops? Plant. Physiol. 2011;156:1058–1066. doi: 10.1104/pp.111.174318. PubMed DOI PMC

Chapin III F.S., Kedrowski R.A. Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology. 1983;64:376–391. doi: 10.2307/1937083. DOI

Ågren G.I., Wetterstedt J., Billberger M.F.K. Nutrient limitation on terrestrial plant growth--modeling the interaction between nitrogen and phosphorus. New Phytol. 2012;194:953–960. doi: 10.1111/j.1469-8137.2012.04116.x. PubMed DOI

Veneklaas E.J., Lambers H., Bragg J., Finnegan P.M., Lovelock C.E., Plaxton W.C., Price C.A., Scheible W.-R., Shane M.W., White P.J., et al. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol. 2012;195:306–320. doi: 10.1111/j.1469-8137.2012.04190.x. PubMed DOI

Elser J.J., Brien W.J.O., Dobberfuhl D.R., Dowling T.E. The evolution of ecosystem processes: Growth rate and elemental stoichiometry of a key herbivore in temperate and arctic habitats. J. Evol. Biol. 2000;13:845–853. doi: 10.1046/j.1420-9101.2000.00215.x. DOI

Schlüter U., Colmsee C., Scholz U., Bräutigam A., Weber A.P.M., Zellerhoff N., Bucher M., Fahnenstich H., Sonnewald U. Adaptation of maize source leaf metabolism to stress related disturbances in carbon, nitrogen and phosphorus balance. BMC Genom. 2013;14:442. doi: 10.1186/1471-2164-14-442. PubMed DOI PMC

Turner B.L., Mahieu N., Condron L.M. Phosphorus-31 nuclear magnetic resonance spectral assignments of phosphorus compounds in soil NaOH–EDTA extracts. Soil Sci. Soc. Am. J. 2003;67:497–510. doi: 10.2136/sssaj2003.4970. DOI

Cade-Menun B.J., Liu C.W., Nunlist R., McColl J.G. Soil and litter Phosphorus-31 nuclear magnetic resonance spectroscopy. J. Environ. Qual. 2002;31:457–465. PubMed

Vincent A.G., Turner B.L., Tanner E.V.J. Soil organic phosphorus dynamics following perturbation of litter cycling in a tropical moist forest. Eur. J. Soil Sci. 2010;61:48–57. doi: 10.1111/j.1365-2389.2009.01200.x. DOI

Vestergren J., Vincent A.G., Jansson M., Persson P., Ilstedt U., Giesler R. High-resolution characterization of organic phosphorus in soil extracts using 2D 1 H−31 P NMR correlation spectroscopy. Environ. Sci. Technol. 2012;46:3950–3956. doi: 10.1021/es204016h. PubMed DOI

Me Chave J.R., Ra B.R., 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; Paris, France: 2004.

Courtois E.A., Stahl C., Van den Berge J., Bréchet L., Van Langenhove L., Richter A., Urbina I., Soong J.L., Peñuelas J., Janssens I.A. Spatial variation of soil CO2, CH4 and N2O fluxes across topographical positions in tropical forests of the guiana shield. Ecosystems. 2018;21:1445–1458. doi: 10.1007/s10021-018-0232-6. DOI

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

Deborde C., Moing A., Roch L., Jacob D., Rolin D., Giraudeau P. Plant metabolism as studied by NMR Spectrosc. Prog. Nucl. Magn. Reson. Spectrosc. 2017;102–103:61–97. doi: 10.1016/j.pnmrs.2017.05.001. PubMed DOI

Wilson I.D., Plumb R., Granger J., Major H., Williams R., Lenz E.M. 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

Cade-Menun B.J., Preston C.M. A comparison of soil extraction procedures for 31P NMR spectroscopy. Soil Sci. 1996;161:770–785. doi: 10.1097/00010694-199611000-00006. DOI

Makarov M.I., Haumaier L., Zech W., Marfenina O.E., Lysak L.V. Can 31P NMR spectroscopy be used to indicate the origins of soil organic phosphates? Soil Biol. Biochem. 2005;37:15–25. doi: 10.1016/j.soilbio.2004.07.022. DOI

Turner B.L. Soil organic phosphorus in tropical forests: An assessment of the NaOH-EDTA extraction procedure for quantitative analysis by solution 31P NMR spectroscopy. Eur. J. Soil Sci. 2008;59:453–466. doi: 10.1111/j.1365-2389.2007.00994.x. DOI

Smernik R.J., Doolette A.L., Marschner P., Bu E.K., Stonor R., Wakelin S.A., Mcneill A.M. Soil biology & biochemistry forms of phosphorus in bacteria and fungi isolated from two Australian Soils. Soil Biol. Biochem. 2008;40:1908–1915.

Anderson M.J., Gorley R.N., Clarke K.R. PERMANOVA + for PRI-MER: Guide to Software and Statistical Methods. Primer-E; Plymouth, UK: 2008.

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

Williams W.T., Lance G.N., Webb L.J., Tracey J.G., Connell J.H. 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. Clarendon; Oxford, UK: 1975.

Richards P.W. The Tropical Rain Forest; An Ecological Study. Cambridge Univ. Press; New York, NY, USA: 1952.

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

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

Gargallo-Garriga A., Sardans J., Granda V., Llusià J., Peguero G., Asensio D., Ogaya R., Urbina I., Van Langenhove L., Verryckt L.T., et al. Different “metabolomic niches” of the highly diverse tree species of the French Guiana rainforests. Sci. Rep. 2020;10:1–10. doi: 10.1038/s41598-020-63891-y. PubMed DOI PMC

Penuelas J., Sardans J., Llusià J., Owen S.M., Carnicer J., Giambelluca T.W., Rezende E.L., Waite M., Niinemets Ü. Faster returns on ‘leaf economics’ and different biogeochemical niche in invasive compared with native plant species. Glob. Chang. Biol. 2010;16:2171–2185. doi: 10.1111/j.1365-2486.2009.02054.x. DOI

Peñuelas J., Fernández-Martinez M., Ciais P., Jou D., Piao S., Obersteiner M., Vicca S., Janssens I.A., Sardans J. The bioelements, the elementome, and the biogeochemical niche. Ecology. 2019;100:e02652. doi: 10.1002/ecy.2652. PubMed DOI

Sardans J., Janssens I.A., Alonso R., Veresoglou S.D., Rillig M.C., Sanders T.G., Carnicer J., Filella I., Farré-Armengol G., Peñuelas J. 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

Urbina I., Sardans J., Grau O., Beierkuhnlein C., Jentsch A., Kreyling J., Peñuelas J. Plant community composition affects the species biogeochemical niche. Ecosphere. 2017;8:e01801. doi: 10.1002/ecs2.1801. DOI

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

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