Root exudate metabolomes change under drought and show limited capacity for recovery
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
610028
European Research Council - International
ERC-2013-SyG-610028
EC | European Research Council (ERC) - International
ERC-2013-SyG-610028
European Council of International Schools (ECIS) - International
PubMed
30140025
PubMed Central
PMC6107494
DOI
10.1038/s41598-018-30150-0
PII: 10.1038/s41598-018-30150-0
Knihovny.cz E-zdroje
- MeSH
- dub (rod) metabolismus MeSH
- kořeny rostlin metabolismus MeSH
- metabolom fyziologie MeSH
- období sucha MeSH
- rostlinné exsudáty metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- rostlinné exsudáty MeSH
Root exudates comprise a large variety of compounds released by plants into the rhizosphere, including low-molecular-weight primary metabolites (particularly saccharides, amino acids and organic acids) and secondary metabolites (phenolics, flavonoids and terpenoids). Changes in exudate composition could have impacts on the plant itself, on other plants, on soil properties (e.g. amount of soil organic matter), and on soil organisms. The effects of drought on the composition of root exudates, however, have been rarely studied. We used an ecometabolomics approach to identify the compounds in the exudates of Quercus ilex (holm oak) under an experimental drought gradient and subsequent recovery. Increasing drought stress strongly affected the composition of the exudate metabolome. Plant exudates under drought consisted mainly of secondary metabolites (71% of total metabolites) associated with plant responses to drought stress, whereas the metabolite composition under recovery shifted towards a dominance of primary metabolites (81% of total metabolites). These results strongly suggested that roots exude the most abundant root metabolites. The exudates were changed irreversibly by the lack of water under extreme drought conditions, and the plants could not recover.
CREAF Cerdanyola del Vallès 08193 Catalonia Spain
CSIC Global Ecology Unit CREAF CSIC UAB Bellaterra 08193 Catalonia Spain
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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
Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Micro. 2013;11:789–799. doi: 10.1038/nrmicro3109. PubMed DOI
Zhu B, et al. Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biol. Biochem. 2014;76:183–192. doi: 10.1016/j.soilbio.2014.04.033. DOI
Keiluweit M, et al. Mineral protection of soil carbon counteracted by root exudates. Nat. Clim. Chang. 2015;5:588–595. doi: 10.1038/nclimate2580. DOI
Rousk K, Michelsen A, Rousk J. Microbial control of soil organic matter mineralization responses to labile carbon in subarctic climate change treatments. Glob. Chang. Biol. 2016;22:4150–4161. doi: 10.1111/gcb.13296. PubMed DOI
Badri DV, Vivanco JM. Regulation and function of root exudates. Plant. Cell Environ. 2009;32:666–681. doi: 10.1111/j.1365-3040.2009.01926.x. PubMed DOI
Baetz U, Martinoia E. Root exudates: The hidden part of plant defense. Trends Plant Sci. 2014;19:90–98. doi: 10.1016/j.tplants.2013.11.006. PubMed DOI
Dakora FD, Phillips DA. Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil. 2002;245:35–47. doi: 10.1023/A:1020809400075. DOI
Faure D, Vereecke D, Leveau JHJ. Molecular communication in the rhizosphere. Plant Soil. 2009;321:279–303. doi: 10.1007/s11104-008-9839-2. DOI
Jones DL, Hodge A, Kuzyakov Y. Plant and mycorrhizal regulation of rhizodeposition. New Phytol. 2004;163:459–480. doi: 10.1111/j.1469-8137.2004.01130.x. PubMed DOI
Pinton, R., Varanini, Z. & Nannipieri, P. The rhizosphere: biochemistry and organic substances at the soil-plant interface. (CRC press, 2007).
Jones DL, Nguyen C, Finlay RD. Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil. 2009;321:5–33. doi: 10.1007/s11104-009-9925-0. DOI
Kuzyakov Y, Domanski G. Carbon input by plants into the soil. Review. J. Plant Nutr. Soil Sci. 2000;163:421–431. doi: 10.1002/1522-2624(200008)163:4<421::AID-JPLN421>3.0.CO;2-R. DOI
Ma JF, Ryan PR, Delhaize E. Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 2001;6:273–278. doi: 10.1016/S1360-1385(01)01961-6. PubMed DOI
Hirsch AM, et al. Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms. Ecology. 2003;84:858–868. doi: 10.1890/0012-9658(2003)084[0858:MSARCR]2.0.CO;2. DOI
Rudrappa T, Czymmek KJ, Paré PW, Bais HP. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol. 2008;148:1547–1556. doi: 10.1104/pp.108.127613. PubMed DOI PMC
Gargallo-Garriga A, et al. Shifts in plant foliar and floral metabolomes in response to the suppression of the associated microbiota. BMC Plant Biol. 2016;16:78. doi: 10.1186/s12870-016-0767-7. PubMed DOI PMC
Biedrzycki ML, Jilany TA, Dudley SA, Bais HP. Root exudates mediate kin recognition in plants. Commun. Integr. Biol. 2010;3:28–35. doi: 10.4161/cib.3.1.10118. PubMed DOI PMC
Aulakh MS, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H. Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biol. 2001;3:139–148. doi: 10.1055/s-2001-12905. DOI
Chaparro JM, et al. Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PLoS One. 2013;8:e55731. doi: 10.1371/journal.pone.0055731. PubMed DOI PMC
Neumann G, Römheld V. Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil. 1999;211:121–130. doi: 10.1023/A:1004380832118. DOI
Johnson JF, Allan DL, Vance CP. Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol. 1994;104:657–665. doi: 10.1104/pp.104.2.657. PubMed DOI PMC
Lipton DS, Blanchar RW, Blevins DG. Citrate, malate, and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings. Plant Physiol. 1987;85:315–317. doi: 10.1104/pp.85.2.315. PubMed DOI PMC
Hoffland E, Van Den Boogaard R, Nelemans J, Findenegg G. Biosynthesis and root exudation of citric and malic acids in phosphate-starved rape plants. New Phytol. 1992;122:675–680. doi: 10.1111/j.1469-8137.1992.tb00096.x. DOI
Li YP, Ye W, Wang M, Yan XD. Climate change and drought: a risk assessment of crop-yield impacts. Clim. Res. 2009;39:31–46. doi: 10.3354/cr00797. DOI
Dai A. Drought under global warming: a review. Wiley Interdiscip. Rev. Clim. Chang. 2011;2:45–65. doi: 10.1002/wcc.81. DOI
Ryan MG. Tree responses to drought. Tree Physiol. 2011;31:237–239. doi: 10.1093/treephys/tpr022. PubMed DOI
Harfouche A, Meilan R, Altman A. Molecular and physiological responses to abiotic stress in forest trees and their relevance to tree improvement. Tree Physiol. 2014;34:1181–1198. doi: 10.1093/treephys/tpu012. PubMed DOI
Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C. How tree roots respond to drought. Front. Plant Sci. 2015;6:547. doi: 10.3389/fpls.2015.00547. PubMed DOI PMC
Cuneo IF, Knipfer T, Brodersen CR, McElrone AJ. Mechanical Failure of Fine Root Cortical Cells Initiates Plant Hydraulic Decline during Drought. Plant Physiol. 2016;172:1669–1678. doi: 10.1104/pp.16.00923. PubMed DOI PMC
Preece C, Peñuelas J. Rhizodeposition under drought and consequences for soil communities and ecosystem resilience. Plant Soil. 2016;409:1–17. doi: 10.1007/s11104-016-3090-z. DOI
Preece, C., Farré-Armengol, G., Llusià, J. & Peñuelas, J. Thirsty tree roots exude more carbon. Tree Physiol. 38(5), 690–695 10.1093/treephys/tpx163 (2018). PubMed
Czarnes S, Hallett PD, Bengough AG, Young IM. Root- and microbial-derived mucilages affect soil structure and water transport. Eur. J. Soil Sci. 2000;51:435–443. doi: 10.1046/j.1365-2389.2000.00327.x. DOI
Ahmed MA, Kroener E, Holz M, Zarebanadkouki M, Carminati A. Mucilage exudation facilitates root water uptake in dry soils. Funct. Plant Biol. 2014;41:1129–1137. doi: 10.1071/FP13330. PubMed DOI
Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A. Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytol. 2014;201:916–927. doi: 10.1111/nph.12569. PubMed DOI PMC
Dyer CL, Kopittke PM, Sheldon AR, Menzies NW. Influence of soil moisture content on soil solution composition. Soil Sci. Soc. Am. J. 2008;72:355–361. doi: 10.2136/sssaj2007.0124. DOI
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
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
Canarini A, Dijkstra FA. Dry-rewetting cycles regulate wheat carbon rhizodeposition, stabilization and nitrogen cycling. Soil Biol. Biochem. 2015;81:195–203. doi: 10.1016/j.soilbio.2014.11.014. DOI
Song FB, Han XY, Zhu XC, Herbert SJ. Response to water stress of soil enzymes and root exudates from drought and non-drought tolerant corn hybrids at different growth stages. Can. J. Soil Sci. 2012;92:501–507. doi: 10.4141/cjss2010-057. DOI
Henry A, Doucette W, Norton J, Bugbee B. Changes in crested wheatgrass root exudation caused by flood, drought, and nutrient stress. J. Environ. Qual. 2007;36:904–912. doi: 10.2134/jeq2006.0425sc. PubMed DOI
van Dam NM, Bouwmeester HJ. Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci. 2016;21:256–265. doi: 10.1016/j.tplants.2016.01.008. PubMed DOI
Valentinuzzi F, et al. Phosphorus and iron defciencies induce a metabolic reprogramming and affect the exudation traits of the woody plant Fragaria x ananassa. J. Exp. Bot. 2015;66:6483–6495. doi: 10.1093/jxb/erv364. PubMed DOI
Zubair HM, Pratley JE, Sandral GA, Humphries A. Allelopathic interference of alfalfa (Medicago sativa L.) genotypes to annual ryegrass (Lolium rigidum) J. Plant Res. 2017;130:647–658. doi: 10.1007/s10265-017-0921-9. PubMed DOI
Canarini A, Merchant A, Dijkstra FA. Drought effects on Helianthus annuus and Glycine max metabolites: from phloem to root exudates. Rhizosphere. 2016;2:85–97. doi: 10.1016/j.rhisph.2016.06.003. DOI
Peñuelas J, Sardans J. Ecological metabolomics. Chem. Ecol. 2009;25:305–309. doi: 10.1080/02757540903062517. 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
Fiehn O. Metabolomics–the link between genotypes and phenotypes. Plant Mol. Biol. 2002;48:155–71. doi: 10.1023/A:1013713905833. PubMed 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
Lloret F, Peñuelas J, Ogaya R. Establishment of co-existing Mediterranean tree species under a varying soil moisture regime. J. Veg. Sci. 2004;15:237–244. doi: 10.1111/j.1654-1103.2004.tb02258.x. DOI
Sánchez-Humanes, B. & Espelta, J. M. Increased drought reduces acorn production in Quercus ilex coppices: thinning mitigates this effect but only in the short term. Forestry, 10.1093/forestry/cpq045 (2011).
Rivas-Ubach A, et al. Drought enhances folivory by shifting foliar metabolomes in Quercus ilex trees. New Phytol. 2014;202:874–85. doi: 10.1111/nph.12687. PubMed DOI
Angelica MD, Fong Y. NIH Public Access. October. 2008;141:520–529.
Curiel-Yuste J, et al. Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Glob. Chang. Biol. 2011;17:1475–1486. doi: 10.1111/j.1365-2486.2010.02300.x. DOI
Dam NMV, Bouwmeester HJ. Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci. 2016;21(3):256–265. doi: 10.1016/j.tplants.2016.01.008. PubMed DOI
Bilgin DD, et al. Biotic stress globally downregulates photosynthesis genes. Plant, Cell Environ. 2010;33:1597–1613. doi: 10.1111/j.1365-3040.2010.02167.x. PubMed DOI
Wilkinson S, Davies WJ. ABA-based chemical signalling: The co-ordination of responses to stress in plants. Plant, Cell Environ. 2002;25:195–210. doi: 10.1046/j.0016-8025.2001.00824.x. PubMed DOI
Wilkinson S, Davies WJ. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant, Cell Environ. 2010;33:510–525. doi: 10.1111/j.1365-3040.2009.02052.x. PubMed DOI
Davies WJ, Zhang JH. Root signals and the regulation of growth and development of plants in drying soil. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991;42:55–76. doi: 10.1146/annurev.pp.42.060191.000415. DOI
McAdam SAM, Manzi M, Ross JJ, Brodribb TJ, Gómez-Cadenas A. Uprooting an abscisic acid paradigm: Shoots are the primary source. Plant Signal. Behav. 2016;11:e1169359. doi: 10.1080/15592324.2016.1169359. PubMed DOI PMC
Manzi M, Pitarch-Bielsa M, Arbona V, Gomez-Cadenas A. Leaf dehydration is needed to induce abscisic acid accumulation in roots of citrus plants. Environ. Exp. Bot. 2017;139:116–126. doi: 10.1016/j.envexpbot.2017.05.004. DOI
de Ollas C, Arbona V, Gómez-Cadenas A. Jasmonoyl isoleucine accumulation is needed for abscisic acid build-up in roots of Arabidopsis under water stress conditions. Plant, Cell Environ. 2015;38:2157–2170. doi: 10.1111/pce.12536. PubMed DOI
Sardans J, et al. Metabolic responses of Quercus ilex seedlings to wounding analysed with nuclear magnetic resonance profiling. Plant Biol. 2013;2:1–9. PubMed
Li Z, Yu J, Peng Y, Huang B. Metabolic pathways regulated by abscisic acid, salicylic acid and γ-aminobutyric acid in association with improved drought tolerance in creeping bentgrass (Agrostis stolonifera) Physiol. Plant. 2017;159:42–58. doi: 10.1111/ppl.12483. PubMed DOI
Li X, Dong J, Chu W, Chen Y. The relationship between root exudation properties and root morphological traits of cucumber grown under different nitrogen supplies and atmospheric CO 2 concentrations. Plant Soil. 2018;425:415–432. doi: 10.1007/s11104-017-3555-8. DOI
Lesuffleur F, Cliquet JB. Characterisation of root amino acid exudation in white clover (Trifolium repens L.) Plant Soil. 2010;333:191–201. doi: 10.1007/s11104-010-0334-1. DOI
Good AG, Zaplachinski ST. The effects of drought stress on free amino acid accumulation and protein synthesis in Brassica napus. Physiol. Plant. 1994;90:9–14. doi: 10.1111/j.1399-3054.1994.tb02185.x. DOI
De Diego N, et al. Solute accumulation and elastic modulus changes in six radiata pine breeds exposed to drought. Tree Physiol. 2013;33:69–80. doi: 10.1093/treephys/tps125. PubMed DOI
Wu GQ, Feng RJ, Shui QZ. Effect of osmotic stress on growth and osmolytes accumulation in sugar beet (Beta vulgaris L.) plants. Plant Soil Environ. 2016;62:189–194. doi: 10.17221/101/2016-PSE. DOI
Hare PD, Cress WA, Van Staden J. Dissecting the roles of osmolyte accumulation during stress. Plant. Cell Environ. 1998;21:535–553. doi: 10.1046/j.1365-3040.1998.00309.x. DOI
Serraj R, Sinclair TR. Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant. Cell Environ. 2002;25:333–341. doi: 10.1046/j.1365-3040.2002.00754.x. PubMed DOI
Blum A. Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ. 2017;40:4–10. doi: 10.1111/pce.12800. PubMed DOI
Gregorová Z, et al. Drought-induced responses of physiology, metabolites, and PR proteins in Triticum aestivum. J. Agric. Food Chem. 2015;63:8125–8133. doi: 10.1021/acs.jafc.5b02951. PubMed DOI
Chmielewska K, et al. Analysis of drought-induced proteomic and metabolomic changes in barley (Hordeum vulgare L.) leaves and roots unravels some aspects of biochemical mechanisms involved in drought tolerance. Front. Plant Sci. 2016;7:14. doi: 10.3389/fpls.2016.01108. PubMed DOI PMC
Bhaskara GB, Yang T-H, Verslues PE. Dynamic proline metabolism: importance and regulation in water limited environments. Front. Plant Sci. 2015;6:484. doi: 10.3389/fpls.2015.00484. PubMed DOI PMC
Macková H, et al. Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J. Exp. Bot. 2013;64:2805–2815. doi: 10.1093/jxb/ert131. PubMed DOI PMC
Xu, Y., Burgess, P. & Huang, B. Transcriptional regulation of hormone-synthesis and signaling pathways by overexpressing cytokinin-synthesis contributes to improved drought tolerance in creeping bentgrass. Physiol. Plant. 161(2), 235–256. 10.1111/ppl.12588 (2017). PubMed
Kang Y, et al. System responses to long-term drought and re-watering of two contrasting alfalfa varieties. Plant J. 2011;68:871–889. doi: 10.1111/j.1365-313X.2011.04738.x. PubMed DOI
Agati G, Azzarello E, Pollastri S, Tattini M. Flavonoids as antioxidants in plants: Location and functional significance. Plant Sci. 2012;196:67–76. doi: 10.1016/j.plantsci.2012.07.014. PubMed DOI
Peñuelas J, Estiarte M, Kimball B. Flavonoid responses in wheat grown at elevated CO2: green versus senescent leaves. Photosynthetica. 1999;37:615–619. doi: 10.1023/A:1007131827115. DOI
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
Kape R, et al. Chemotaxis and nod Gene Activity of Bradyrhizobium japonicum in Response to Hydroxycinnamic Acids and Isoflavonoids. Appl. Environ. Microbiol. 1991;57:316–319. PubMed PMC
Stafford HA. Roles of Flavonoids in Symbiotic and Defense Functions in Legume Roots. Bot. Rev. 1997;63:27–39. doi: 10.1007/BF02857916. DOI
Aoki T, Akashi T, Ayabe S. Flavonoids of Leguminous Plants: Structure, Biological Activity, and Biosynthesis. J. Plant Res. 2000;113:475–488. doi: 10.1007/PL00013958. DOI
Forkmann G, Martens S. Metabolic engineering and applications of flavonoids. Curr. Opin. Biotechnol. 2001;12:155–160. doi: 10.1016/S0958-1669(00)00192-0. PubMed DOI
Watson BS, et al. Integrated Metabolomics and Transcriptomics Reveal Enhanced Specialized Metabolism in Medicago truncatula Root Border Cells. Plant Physiol. 2015;167:1699–1716. doi: 10.1104/pp.114.253054. PubMed DOI PMC
Zhang, J., Chen, G., Zhao, P., Zhou, Q. & Zhao, X. The abundance of certain metabolites responds to drought stress in the highly drought tolerant plant Caragana korshinskii. Acta Physiol. Plant. 39 (2017).
Ta TC, Joy KW, Ireland R. Role of asparagine in the photochemistry nitrogen metaboliem of pea leaves. Plant Physiol. 1985;78:334–337. doi: 10.1104/pp.78.2.334. PubMed DOI PMC
Zhang C, Preece C, Filella I, Farré-Armengol G, Peñuelas J. Assessment of the response of photosynthetic activity of Mediterranean evergreen oaks to enhanced drought stress and recovery by using PRI and R690/R630. Forests. 2017;8:386–390. doi: 10.3390/f8100386. DOI
Souza RP, Machado EC, Silva JAB, Lagôa AMMA, Silveira JAG. Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environ. Exp. Bot. 2004;51:45–56. doi: 10.1016/S0098-8472(03)00059-5. DOI
Miyashita K, Tanakamaru S, Maitani T, Kimura K. Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress. Environ. Exp. Bot. 2005;53:205–214. doi: 10.1016/j.envexpbot.2004.03.015. DOI
Peñuelas, J. et al. Assessment of the impacts of climate change on Mediterranean terrestrial ecosystems based on data from field experiments and long-term monitored field gradients in Catalonia. Environmental and Experimental Botany152, 49–59 10.1016/j.envexpbot.2017.05.012 (2018).
Genty B, Jean-Marie B, Neil R. B. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta (BBA)-General Subj. 1989;990:87–92. doi: 10.1016/S0304-4165(89)80016-9. DOI