Rhizodeposition under drought and consequences for soil communities and ecosystem resilience

Abstract

Background

Rhizodeposition is the release of organic compounds from plant roots into soil. Positive relationships between rhizodeposition and soil microbial biomass are commonly observed. Rhizodeposition may be disrupted by increasing drought however the effects of water stress on this process are not sufficiently understood.

Scope

We aimed to provide a synthesis of the current knowledge of drought impacts on rhizodeposition. The current scarcity of well-defined studies hinders a quantitative meta-analysis, but we are able to identify the main effects of water stress on this process and how changes in the severity of drought may produce different responses. We then give an overview of the links between rhizodeposition and microbial communities, and describe how drought may disrupt these interactions.

Conclusions

Overall, moderate drought appears to increase rhizodeposition per gram of plant, but under extreme drought rhizodeposition is more variable. Concurrent decreases in plant biomass may lessen the total amount of rhizodeposits entering the soil. Effects on rhizodeposition may be strongly species-dependant therefore impacts on soil communities may also vary, either driving subsequent changes or conferring resilience in the plant community. Advances in the study of rhizodeposition are needed to allow a deeper understanding of this plant-soil interaction and how it will respond to drought.

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References

  1. Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci 105:11512–11519. doi:10.1073/pnas.0801925105

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  2. Asmar F, Eiland F, Nielsen NE (1994) Effect of extracellular-enzyme activities on solubilization rate of soil organic nitrogen. Biol Fertil Soils 17:32–38. doi:10.1007/bf00418669

    CAS  Article  Google Scholar 

  3. Averill C, Waring BG, Hawkes CV (2016) Historical precipitation predictably alters the shape and magnitude of microbial functional response to soil moisture. Glob Chang Biol 22:1957–1964. doi:10.1111/gcb.13219

    PubMed  Article  Google Scholar 

  4. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interations with plants and other organisms. Annual Review of Plant Biology.

    Google Scholar 

  5. Bakker PA, Berendsen RL, Doornbos RF, Wintermans PC, Pieterse CM (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4

  6. Baptist F, Aranjuelo I, Legay N, Lopez-Sangil L, Molero G, Rovira P, Nogues S (2015) Rhizodeposition of organic carbon by plants with contrasting traits for resource acquisition: responses to different fertility regimes. Plant Soil 394:391–406. doi:10.1007/s11104-015-2531-4

    CAS  Article  Google Scholar 

  7. Bardgett RD, Manning P, Morrien E, De Vries FT (2013) Hierarchical responses of plant-soil interactions to climate change: consequences for the global carbon cycle. J Ecol 101:334–343. doi:10.1111/1365-2745.12043

    Article  Google Scholar 

  8. Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699. doi:10.1016/j.tree.2014.10.006

    PubMed  Article  Google Scholar 

  9. Barthès B, Roose E (2002) Aggregate stability as an indicator of soil susceptibility to runoff and erosion; validation at several levels. Catena 47:133–149. doi:10.1016/S0341-8162(01)00180-1

    Article  Google Scholar 

  10. Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol 181:413–423. doi:10.1111/j.1469-8137.2008.02657.x

    CAS  PubMed  Article  Google Scholar 

  11. Benizri E, Nguyen C, Piutti S, Slezack-Deschaumes S, Philippot L (2007) Additions of maize root mucilage to soil changed the structure of the bacterial community. Soil Biol Biochem 39:1230–1233. doi:10.1016/j.soilbio.2006.12.026

    CAS  Article  Google Scholar 

  12. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13. doi:10.1111/j.1574-6941.2009.00654.x

    CAS  PubMed  Article  Google Scholar 

  13. Blum A (1989) Osmotic adjustment and growth of barley genotypes under drought stress. Crop Sci 29:230–233

    Article  Google Scholar 

  14. Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811. doi:10.1016/j.femsre. 2004.11.005

    PubMed  Article  CAS  Google Scholar 

  15. Bota J, Medrano H, Flexas J (2004) Is photosynthesis limited by decreased rubisco activity and RuBP content under progressive water stress? New Phytol 162:671–681. doi:10.1111/j.1469-8137.2004.01056.x

    CAS  Article  Google Scholar 

  16. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744. doi:10.1128/aem.02188-07

    CAS  PubMed  Article  Google Scholar 

  17. Bronick CJ, Lal R (2005) Soil structure and management: a review. Geoderma 124:3–22. doi:10.1016/j.geoderma. 2004.03.005

    CAS  Article  Google Scholar 

  18. Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:547. doi:10.3389/fpls.2015.00547

    PubMed  PubMed Central  Article  Google Scholar 

  19. Brzostek ER, Greco A, Drake JE, Finzi AC (2013) Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry 115:65–76. doi:10.1007/s10533-012-9818-9

    CAS  Article  Google Scholar 

  20. Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. doi:10.1146/annurev-arplant-050312-120106

    CAS  PubMed  Article  Google Scholar 

  21. Canarini A, Dijkstra FA (2015) Dry-rewetting cycles regulate wheat carbon rhizodeposition, stabilization and nitrogen cycling. Soil Biol Biochem 81:195–203. doi:10.1016/j.soilbio.2014.11.014

    CAS  Article  Google Scholar 

  22. Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei M-R, Borriss R, von Wirén N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J Plant Nutr Soil Sci 174:3–11. doi:10.1002/jpln.201000085

    CAS  Article  Google Scholar 

  23. Chaves MM (1991) Effects of water deficits on carbon assimilation. J Exp Bot 42:1–16. doi:10.1093/jxb/42.1.1

    CAS  Article  Google Scholar 

  24. Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384. doi:10.1093/jxb/erh269

    CAS  PubMed  Article  Google Scholar 

  25. Chaves MM, Maroco J, Pereira J (2003) Understanding plant responses to drought — from genes to the whole plant. Funct Plant Biol 30:239–264. doi:10.1071/FP02076

    CAS  Article  Google Scholar 

  26. Cheng W, Gershenson A (2007) Carbon fluxes in the rhizosphere. In: Cardon ZG, Whitbeck JL (eds) The rhizosphere: an ecological perspective. Elsevier Academic Press, London, UK, p 31–56

  27. Clark JS, Campbell JH, Grizzle H, Acosta-Martinez V, Zak JC (2009) Soil microbial community response to drought and precipitation variability in the Chihuahuan Desert. Microb Ecol 57:248–260. doi:10.1007/s00248-008-9475-7

    PubMed  Article  Google Scholar 

  28. Cruz-Martinez K, Suttle KB, Brodie EL, Power ME, Andersen GL, Banfield JF (2009) Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland. ISME J 3:738–744 http://www.nature.com/ismej/journal/v3/n6/suppinfo/ismej200916s1.html

    CAS  PubMed  Article  Google Scholar 

  29. Curiel Yuste J, Fernandez-Gonzalez AJ, Fernandez-Lopez M, Ogaya R, Penuelas J, Sardans J, Lloret F (2014) Strong functional stability of soil microbial communities under semiarid Mediterranean conditions and subjected to long-term shifts in baseline precipitation. Soil Biol Biochem 69:223–233. doi:10.1016/j.soilbio.2013.10.045

    CAS  Article  Google Scholar 

  30. Czarnes S, Hallett PD, Bengough AG, Young IM (2000) Root- and microbial-derived mucilages affect soil structure and water transport. Eur J Soil Sci 51:435–443. doi:10.1046/j.1365-2389.2000.00327.x

    Article  Google Scholar 

  31. Dai A (2011) Drought under global warming: a review. Wiley Interdiscip Rev Clim Chang 2:45–65. doi:10.1002/wcc.81

    Article  Google Scholar 

  32. Dannenmann M, Simon J, Gasche R, Holst J, Naumann PS, Kögel-Knabner I, Knicker H, Mayer H, Schloter M, Pena R, Polle A, Rennenberg H, Papen H (2009) Tree girdling provides insight on the role of labile carbon in nitrogen partitioning between soil microorganisms and adult European beech. Soil Biol Biochem 41:1622–1631. doi:10.1016/j.soilbio.2009.04.024

    CAS  Article  Google Scholar 

  33. Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, Berdugo M, Campbell CD, Singh BK (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7. doi:10.1038/ncomms10541

  34. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327. doi:10.1111/j.1574-6941.2010.00860.x

    CAS  PubMed  Article  Google Scholar 

  35. Dijkstra FA, Cheng WX (2007) Moisture modulates rhizosphere effects on C decomposition in two different soil types. Soil Biol Biochem 39:2264–2274. doi:10.1016/j.soilbio.2007.03.026

    CAS  Article  Google Scholar 

  36. Dijkstra FA, Cheng W, Johnson DW (2006) Plant biomass influences rhizosphere priming effects on soil organic matter decomposition in two differently managed soils. Soil Biol Biochem 38:2519–2526. doi:10.1016/j.soilbio.2006.02.020

    CAS  Article  Google Scholar 

  37. Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:8. doi:10.3389/fmicb.2013.00216

    Article  CAS  Google Scholar 

  38. Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Resour 30:75–115. doi:10.1146/annurev.energy.30.050504.144212

    Article  Google Scholar 

  39. Eilers KG, Lauber CL, Knight R, Fierer N (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896–903. doi:10.1016/j.soilbio.2010.02.003

    CAS  Article  Google Scholar 

  40. Evans SE, Wallenstein MD (2012) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109:101–116. doi:10.1007/s10533-011-9638-3

    Article  Google Scholar 

  41. Feeney DS, Crawford JW, Daniell T, Hallett PD, Nunan N, Ritz K, Rivers M, Young IM (2006) Three-dimensional microorganization of the soil–root–microbe system. Microb Ecol 52:151–158

    PubMed  Article  Google Scholar 

  42. Field CB, Barros VR, Mach KJ, Mastrandrea MD, Mv A, Adger WN, Arent DJ, Barnett J, Betts R, Bilir TE, Birkmann J, Carmin J, Chadee DD, Challinor AJ, Chatterjee M, Cramer W, Davidson DJ, Estrada YO, Gattuso JP, Hijioka Y, Hoegh-Guldberg O, Huang HQ, Insarov GE, Jones RN, Kovats RS, Lankao PR, Larsen JN, Losada IJ, Marengo JA, McLean RF, Mearns LO, Mechler R, Morton JF, Niang I, Oki T, Olwoch JM, Opondo M, Poloczanska ES, Pörtner HO, Redsteer MH, Reisinger A, Revi A, Schmidt DN, Shaw MR, Solecki W, Stone DA, Stone JMR, Strzepek KM, Suarez AG, Tschakert P, Valentini R, Vicuña S, Villamizar A, Vincent KE, Warren R, White LL, Wilbanks TJ, Wong PP, Yohe GW (2014) Technical summary. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Climate change 2014: impacts, adaptation, and vulnerability part a: global and sectoral aspects contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA

    Google Scholar 

  43. Fierer N, Schimel JP, Holden PA (2003) Influence of drying-rewetting frequency on soil bacterial community structure. Microb Ecol 45:63–71. doi:10.1007/s00248-002-1007-2

    CAS  PubMed  Article  Google Scholar 

  44. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    PubMed  Article  Google Scholar 

  45. Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA, Kramer MA, Phillips RP (2015) Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob Chang Biol 21:2082–2094. doi:10.1111/gcb.12816

    PubMed  Article  Google Scholar 

  46. Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol 6:269–279. doi:10.1055/s-2004-820867

    CAS  PubMed  Article  Google Scholar 

  47. Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A (2014) 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 201:916–927. doi:10.1111/nph.12569

    CAS  PubMed  Article  Google Scholar 

  48. Gargallo-Garriga A, Sardans J, Pérez-Trujillo M, Rivas-Ubach A, Oravec M, Vecerova K, Urban O, Jentsch A, Kreyling J, Beierkuhnlein C, Parella T, Peñuelas J (2014) Opposite metabolic responses of shoots and roots to drought. Sci Report 4:6829. doi:10.1038/srep06829 http://www.nature.com/articles/srep06829#supplementary-information

    CAS  Article  Google Scholar 

  49. Gaul D, Hertel D, Borken W, Matzner E, Leuschner C (2008) Effects of experimental drought on the fine root system of mature Norway spruce. For Ecol Manag 256:1151–1159. doi:10.1016/j.foreco.2008.06.016

    Article  Google Scholar 

  50. Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242. doi:10.1080/07352680701572966

    CAS  Article  Google Scholar 

  51. Gorissen A, Tietema A, Joosten NN, Estiarte M, Peñuelas J, Sowerby A, Emmett BA, Beier C (2004) Climate change affects carbon allocation to the soil in shrublands. Ecosystems 7:650–661. doi:10.1007/s10021-004-0218-4

    CAS  Article  Google Scholar 

  52. Grassi G, Magnani F (2005) Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell Environ 28:834–849. doi:10.1111/j.1365-3040.2005.01333.x

    CAS  Article  Google Scholar 

  53. Gregory PJ (2006) Roots, rhizosphere and soil: the route to a better understanding of soil science? Eur J Soil Sci 57:2–12. doi:10.1111/j.1365-2389.2005.00778.x

    Article  Google Scholar 

  54. Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37:112–129. doi:10.1111/j.1574-6976.2012.00343.x

    CAS  PubMed  Article  Google Scholar 

  55. Griffiths BS, Ritz K, Ebblewhite N, Dobson G (1999) Soil microbial community structure: effects of substrate loading rates. Soil Biol Biochem 31:145–153

    CAS  Article  Google Scholar 

  56. Guggenberger G, Frey SD, Six J, Paustian K, Elliott ET (1999) Bacterial and fungal cell-wall residues in conventional and no-tillage agroecosystems. Soil Sci Soc Am J 63:1188–1198. doi:10.2136/sssaj1999.6351188x

    CAS  Article  Google Scholar 

  57. Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230 http://www.nature.com/ismej/journal/v2/n12/suppinfo/ismej200880s1.html

    CAS  PubMed  Article  Google Scholar 

  58. Hawkes CV, Keitt TH (2015) Resilience vs. historical contingency in microbial responses to environmental change. Ecol Lett 18:612–625. doi:10.1111/ele.12451

    PubMed  Article  Google Scholar 

  59. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis or response ratios in experimental ecology. Ecology 80:1150–1156. doi:10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2

    Article  Google Scholar 

  60. Henry A, Doucette W, Norton J, Bugbee B (2007) Changes in crested wheatgrass root exudation caused by flood, drought, and nutrient stress. J Environ Qual 36:904–912. doi:10.2134/jeq2006.0425sc

    CAS  PubMed  Article  Google Scholar 

  61. Hoffland E, Van Den Boogaard R, Nelemans J, Findenegg G (1992) Biosynthesis and root exudation of citric and malic acids in phosphate-starved rape plants. New Phytol 122:675–680. doi:10.1111/j.1469-8137.1992.tb00096.x

    CAS  Article  Google Scholar 

  62. Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Lofvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792

    PubMed  Article  Google Scholar 

  63. Holling CS (1973) Resilience and stability of ecological systems. Annu Rev Ecol Syst 4:1–23. doi:10.1146/annurev.es.04.110173.000245

    Article  Google Scholar 

  64. Hütsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition: an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165:397–407

    Article  Google Scholar 

  65. Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11:100–105

    Google Scholar 

  66. Johnson JF, Allan DL, Vance CP (1994) Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol 104:657–665. doi:10.1104/pp.104.2.657

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  67. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480. doi:10.1111/j.1469-8137.2004.01130.x

    CAS  Article  Google Scholar 

  68. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321:5–33. doi:10.1007/s11104-009-9925-0

    CAS  Article  Google Scholar 

  69. Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review. J Plant Nutr Soil Sci 163:421–431. doi:10.1002/1522-2624(200008)163:4<421::AID-JPLN421>3.0.CO;2-R

    CAS  Article  Google Scholar 

  70. Lal R (2009) Soil degradation as a reason for inadequate human nutrition. Food Sec 1:45–57. doi:10.1007/s12571-009-0009-z

    Article  Google Scholar 

  71. Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci 109:14058–14062. doi:10.1073/pnas.1202319109

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  72. Li YP, Ye W, Wang M, Yan XD (2009) Climate change and drought: a risk assessment of crop-yield impacts. Clim Res 39:31–46

    CAS  Article  Google Scholar 

  73. Lipton DS, Blanchar RW, Blevins DG (1987) Citrate, malate, and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. Seedlings. Plant Physiol 85:315–317. doi:10.1104/pp.85.2.315

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  74. Loeppmann S, Blagodatskaya E, Pausch J, Kuzyakov Y (2016) Substrate quality affects kinetics and catalytic efficiency of exo-enzymes in rhizosphere and detritusphere. Soil Biol Biochem 92:111–118. doi:10.1016/j.soilbio.2015,09.020

    CAS  Article  Google Scholar 

  75. Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, Abou-Hadid AF, El-Behairy UA, Sorlini C, Cherif A, Zocchi G, Daffonchio D (2012) A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 7:e48479. doi:10.1371/journal.pone.0048479

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  76. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530. doi:10.1016/j.plantsci.2003.10.025

    CAS  Article  Google Scholar 

  77. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739. doi:10.1111/j.1469-8137.2008.02436.x

    PubMed  Article  Google Scholar 

  78. Meharg AA (1994) A critical review of labelling techniques used to quantify rhizosphere carbon-flow. Plant Soil 166:55–62. doi:10.1007/BF02185481

    CAS  Article  Google Scholar 

  79. Mishra AK, Singh VP (2010) A review of drought concepts. J Hydrol 391:202–216. doi:10.1016/j.jhydrol.2010.07.012

    Article  Google Scholar 

  80. Mommer L, Padilla FM, Ruijven J, Caluwe H, Smit-Tiekstra A, Berendse F, Kroon H (2015) Diversity effects on root length production and loss in an experimental grassland community. Funct Ecol 29:1560–1568

    Article  Google Scholar 

  81. Morel JL, Habib L, Plantureux S, Guckert A (1991) Influence of maize root mucilage on soil aggregate stability. Plant Soil 136:111–119. doi:10.1007/bf02465226

    Article  Google Scholar 

  82. Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211:121–130. doi:10.1023/A:1004380832118

    CAS  Article  Google Scholar 

  83. Neumann G, Römheld V (2007) The release of root exudates as affected by the plant physiological status. The Rhizosphere Biochemistry and Organic Substances at the Soil–Plant Interface. 2nd edn. CRC Press/Taylor and Francis, New York

  84. Neumann G, George T, Plassard C (2009) Strategies and methods for studying the rhizosphere—the plant science toolbox. Plant Soil 321:431–456. doi:10.1007/s11104-009-9953-9

    CAS  Article  Google Scholar 

  85. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396

    CAS  Article  Google Scholar 

  86. Nielsen UN, Ayres E, Wall DH, Bardgett RD (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity–function relationships. Eur J Soil Sci 62:105–116. doi:10.1111/j.1365-2389.2010.01314.x

    CAS  Article  Google Scholar 

  87. Oburger E, Schmidt H (2016) New methods to unravel rhizosphere processes. Trends Plant Sci 21:243–255. doi:10.1016/j.tplants.2015.12.005

    CAS  PubMed  Article  Google Scholar 

  88. Oburger E, Dell‘mour M, Hann S, Wieshammer G, Puschenreiter M, WW W (2013) Evaluation of a novel tool for sampling root exudates from soil-grown plants compared to conventional techniques. Environ Exp Bot 87:235–247. doi:10.1016/j.envexpbot.2012.11.007

    Article  Google Scholar 

  89. Palta JA, Gregory PJ (1997) Drought affects the fluxes of carbon to roots and soil in C-13 pulse-labelled plants of wheat. Soil Biol Biochem 29:1395–1403. doi:10.1016/s0038-0717(97)00050-3

    CAS  Article  Google Scholar 

  90. Paterson E (2003) Importance of rhizodeposition in the coupling of plant and microbial productivity. Eur J Soil Sci 54:741–750. doi:10.1046/j.1351-0754.2003.0557.x

    Article  Google Scholar 

  91. Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610. doi:10.1111/j.1469-8137.2006.01931.x

    CAS  PubMed  Article  Google Scholar 

  92. Penuelas J, Prieto P, Beier C, Cesaraccio C, de Angelis P, de Dato G, Emmett BA, Estiarte M, Garadnai J, Gorissen A, Lang EK, Kroel-Dulay G, Llorens L, Pellizzaro G, Riis-Nielsen T, Schmidt IK, Sirca C, Sowerby A, Spano D, Tietema A (2007) Response of plant species richness and primary productivity in shrublands along a north-south gradient in Europe to seven years of experimental warming and drought: reductions in primary productivity in the heat and drought year of 2003. Glob Chang Biol 13:2563–2581. doi:10.1111/j.1365-2486.2007.01464.x

    Article  Google Scholar 

  93. Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894. doi:10.1104/pp.104.044222

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  94. Phillips RP, Erlitz Y, Bier R, Bernhardt ES (2008) New approach for capturing soluble root exudates in forest soils. Funct Ecol 22:990–999. doi:10.1111/j.1365-2435. 2008.01495.x

    Article  Google Scholar 

  95. Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194. doi:10.1111/j.1461-0248.2010.01570.x

    PubMed  Article  Google Scholar 

  96. Pimentel D (2006) Soil erosion: a food and environmental threat. Environ Dev Sustain 8:119–137. doi:10.1007/s10668-005-1262-8

    Article  Google Scholar 

  97. Pinton R, Varanini Z, Nannipieri P (2007) The rhizosphere: biochemistry and organic substances at the soil-plant interface. CRC press

  98. Pollierer MM, Langel R, Körner C, Maraun M, Scheu S (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736. doi:10.1111/j.1461-0248.2007.01064.x

    PubMed  Article  Google Scholar 

  99. R Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  100. Ravenek JM, Bessler H, Engels C, Scherer-Lorenzen M, Gessler A, Gockele A, De Luca E, Temperton VM, Ebeling A, Roscher C (2014) Long-term study of root biomass in a biodiversity experiment reveals shifts in diversity effects over time. Oikos 123:1528–1536

    Article  Google Scholar 

  101. Read DB, Bengough AG, Gregory PJ, Crawford JW, Robinson D, Scrimgeour CM, Young IM, Zhang K, Zhang X (2003) Plant roots release phospholipid surfactants that modify the physical and chemical properties of soil. New Phytol 157:315–326. doi:10.1046/j.1469-8137.2003.00665.x

    CAS  Article  Google Scholar 

  102. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Pierotti Cei F, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331. doi:10.1111/1462-2920.12439

    PubMed  Article  Google Scholar 

  103. Ruf A, Kuzyakov Y, Lopatovskaya O (2006) Carbon fluxes in soil food webs of increasing complexity revealed by 14C labelling and 13C natural abundance. Soil Biol Biochem 38:2390–2400. doi:10.1016/j.soilbio.2006.03.008

    CAS  Article  Google Scholar 

  104. Sanaullah M, Chabbi A, Rumpel C, Kuzyakov Y (2012) Carbon allocation in grassland communities under drought stress followed by C-14 pulse labeling. Soil Biol Biochem 55:132–139. doi:10.1016/j.soilbio.2012.06.004

    CAS  Article  Google Scholar 

  105. Scheunemann N, Digel C, Scheu S, Butenschoen O (2015) Roots rather than shoot residues drive soil arthropod communities of arable fields. Oecologia 179:1135–1145. doi:10.1007/s00442-015-3415-2

    PubMed  Article  Google Scholar 

  106. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394. doi:10.1890/06-0219

    PubMed  Article  Google Scholar 

  107. Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JB (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3:166–181. doi:10.3389/fmicb.2012.00417

    Article  Google Scholar 

  108. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569. doi:10.2136/sssaj2004.0347

    CAS  Article  Google Scholar 

  109. Sobolev VS, Potter TL, Horn BW (2006) Prenylated stilbenes from peanut root mucilage. Phytochem Anal 17:312–322. doi:10.1002/pca.920

    CAS  PubMed  Article  Google Scholar 

  110. Somasundaram S, Rao TP, Tatsumi J, Iijima M (2009) Rhizodeposition of mucilage, root border cells, carbon and water under combined soil physical stresses in Zea mays L. Plant Prod Sci 12:443–448

    Article  Google Scholar 

  111. Song FB, Han XY, Zhu XC, Herbert SJ (2012) 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 92:501–507. doi:10.4141/cjss2010-057

    CAS  Article  Google Scholar 

  112. Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils – methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395. doi:10.1016/j.soilbio.2010.05.007

    CAS  Article  Google Scholar 

  113. Subke J-A, Hahn V, Battipaglia G, Linder S, Buchmann N, Cotrufo MF (2004) Feedback interactions between needle litter decomposition and rhizosphere activity. Oecologia 139:551–559. doi:10.1007/s00442-004-1540-4

    PubMed  Article  Google Scholar 

  114. Svenningsson H, Sundin P, Liljenberg C (1990) Lipids, carbohydrates and amino acids exuded from the axenic roots of rape seedlings exposed to water-deficit stress. Plant Cell Environ 13:155–162. doi:10.1111/j.1365-3040.1990.tb01287.x

    CAS  Article  Google Scholar 

  115. Traore O, Groleau-Renaud V, Plantureux S, Tubeileh A, Boeuf-Tremblay V (2000) Effect of root mucilage and modelled root exudates on soil structure. Eur J Soil Sci 51:575–581. doi:10.1111/j.1365-2389.2000.00348.x

    Article  Google Scholar 

  116. Trap J, Bonkowski M, Plassard C, Villenave C, Blanchart E (2015) Ecological importance of soil bacterivores for ecosystem functions. Plant Soil 398:1–24. doi:10.1007/s11104-015-2671-6

    Article  CAS  Google Scholar 

  117. van Dam NM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21:256–265. doi:10.1016/j.tplants.2016.01.008

    PubMed  Article  CAS  Google Scholar 

  118. Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. doi:10.1111/j.1461-0248.2007.01139.x

    PubMed  Article  Google Scholar 

  119. van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276. doi:10.1111/1365-2745.12054

    Article  Google Scholar 

  120. Vranova V, Rejsek K, Skene KR, Janous D, Formanek P (2013) Methods of collection of plant root exudates in relation to plant metabolism and purpose: a review. J Plant Nutr Soil Sci 176:175–199. doi:10.1002/jpln.201000360

    CAS  Article  Google Scholar 

  121. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003a) Root exudation and rhizosphere biology. Plant Physiol 132:44–51. doi:10.1104/pp.102.019661

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  122. Walker TS, Bais HP, Halligan KM, Stermitz FR, Vivanco JM (2003b) Metabolic profiling of root exudates of Arabidopsis thaliana. J Agric Food Chem 51:2548–2554. doi:10.1021/jf021166h

    CAS  PubMed  Article  Google Scholar 

  123. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. doi:10.1126/science.1094875

    CAS  PubMed  Article  Google Scholar 

  124. Watt M, Evans JR (1999) Proteoid roots. Physiology and development. Plant Physiol 121:317–323. doi:10.1104/pp.121.2.317

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  125. Williams MA (2007) Response of microbial communities to water stress in irrigated and drought-prone tallgrass prairie soils. Soil Biol Biochem 39:2750–2757. doi:10.1016/j.soilbio.2007.05.025

    CAS  Article  Google Scholar 

  126. Xiong YM, D'Atri JJ, Fu SL, Xia HP, Seastedt TR (2011) Rapid soil organic matter loss from forest dieback in a subalpine coniferous ecosystem. Soil Biol Biochem 43:2450–2456. doi:10.1016/j.soilbio.2011.08.013

    CAS  Article  Google Scholar 

  127. Yin H, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221. doi:10.1016/j.soilbio.2014.07.022

    CAS  Article  Google Scholar 

  128. Zang U, Goisser M, Häberle K-H, Matyssek R, Matzner E, Borken W (2014) Effects of drought stress on photosynthesis, rhizosphere respiration, and fine-root characteristics of beech saplings: a rhizotron field study. J Plant Nutr Soil Sci 177:168–177. doi:10.1002/jpln.201300196

    CAS  Article  Google Scholar 

  129. Zeller B, Liu J, Buchmann N, Richter A (2008) Tree girdling increases soil N mineralisation in two spruce stands. Soil Biol Biochem 40:1155–1166. doi:10.1016/j.soilbio.2007.12.009

    CAS  Article  Google Scholar 

  130. Zhao MS, Running SW (2010) Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 329:940–943. doi:10.1126/science.1192666

    CAS  PubMed  Article  Google Scholar 

  131. Zhu B, Cheng WX (2013) Impacts of drying-wetting cycles on rhizosphere respiration and soil organic matter decomposition. Soil Biol Biochem 63:89–96. doi:10.1016/j.soilbio.2013.03.027

    CAS  Article  Google Scholar 

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Acknowledgments

This research was supported by the European FP7 S-Clima project PIEF-GA-2013-626234, the European Research Council Synergy grant ERC-2013-726 SyG-610028 IMBALANCE-P, the Spanish Government project CGL2013-48074-P and the Catalan Government project SGR 2014- 274.

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Correspondence to Catherine Preece.

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Preece, C., Peñuelas, J. Rhizodeposition under drought and consequences for soil communities and ecosystem resilience. Plant Soil 409, 1–17 (2016). https://doi.org/10.1007/s11104-016-3090-z

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Keywords

  • Rhizodeposition
  • Root exudation
  • Drought
  • Soil microbial community
  • Roots
  • Resilience