Plant and Soil

, Volume 423, Issue 1–2, pp 429–442 | Cite as

Rhizodeposition under drought is controlled by root growth rate and rhizosphere water content

  • Maire HolzEmail author
  • Mohsen Zarebanadkouki
  • Anders Kaestner
  • Yakov Kuzyakov
  • Andrea Carminati
Regular Article



Rhizodeposition is an important energy source for soil microorganisms. It is therefore crucial to estimate the distribution of root derived carbon (C) in soil and how it changes with soil water content.


We tested how drought affects exudate distribution in the rhizosphere by coupling 14CO2 labelling of plants and phosphor imaging to estimate C allocation in roots. Rhizosphere water content was visualized by neutron radiography. A numerical model was employed to predict the exudate release and its spatiotemporal distribution along and around growing roots.


Dry and wet plants allocated similar amounts of 14C into roots but root elongation decreased by 48% in dry soil leading to reduced longitudinal rhizosphere extension. Rhizosphere water content was identical (31%) independent of drought, presumably because of the high water retention by mucilage. The model predicted that the increase in rhizosphere water content will enhance diffusion of exudates especially in dry soil and increase their microbial decomposition.


Root growth and rhizosphere water content play an important role in C release by roots and in shaping the profiles of root exudates in the rhizosphere. The release of mucilage may be a plant strategy to maintain fast diffusion of exudates and high microbial activity even under water limitation.


Root exudates Rhizosphere extension Mucilage Convection–diffusion model 14C imaging Neutron radiography 



We acknowledge the DFG for funding (Projects CA 921/3-1 and KU 1184/33-1) and ev. Studienwerk Villigst for funding the position of MH.


  1. Birouste M, Zamora-ledezma E, Bossard C et al (2014) Measurement of fine root tissue density : a comparison of three methods reveals the potential of root dry matter content. Plant Soil 374:299–313. CrossRefGoogle Scholar
  2. Canarini A, Dijkstra FA (2015) Dry-rewetting cycles regulate wheat carbon rhizodeposition, stabilization and nitrogen cycling. Soil Biol Biochem 81:195–203. CrossRefGoogle Scholar
  3. Carminati A, Vetterlein D (2013) Plasticity of rhizosphere hydraulic properties as a key for efficient utilization of scarce resources. Ann Bot 112:277–290. CrossRefPubMedGoogle Scholar
  4. Carminati A, Moradi AB, Vetterlein D et al (2010) Dynamics of soil water content in the rhizosphere. Plant Soil 332:163–176. CrossRefGoogle Scholar
  5. Carminati A, Kroener E, Ahmed MA, et al (2016) Water for carbon, Carbon for Water, Vadose Zo J.
  6. Chaboud A (1983) Isolation, purification and chemical composition of maize root cap slime. Plant Soil 73:395–402CrossRefGoogle Scholar
  7. Chen R, Senbayran M, Blagodatsky S et al (2013) Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Glob Chang Biol 20:2356–2367. CrossRefGoogle Scholar
  8. Darrah PR (1991a) Models of the rhizosphere - II. A quasi three-dimensional simulation of the microbial population dynamics around a growing root releasing soluble exudates. Plant Soil 138:147–158. CrossRefGoogle Scholar
  9. Darrah PR (1991b) Models of the rhizosphere - I. Microbial population dynamics around a root releasing soluble and insoluble carbon. Plant Soil 133:187–199. CrossRefGoogle Scholar
  10. 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. CrossRefPubMedGoogle Scholar
  11. Dilkes N, Jones D, Farrar J (2004) Temporal dynamics of carbon partitioning and rhizodeposition in wheat. Plant Physiol 134:706–715. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84:827–837.[0827:HRCTFO]2.0.CO;2 CrossRefGoogle Scholar
  13. Fuchslueger L, Bahn M, Fritz K et al (2013) 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 201:916–927CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gunina A, Kuzyakov Y (2015) Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate. Soil Biol Biochem 90:87–100. CrossRefGoogle Scholar
  15. Hafner S, Wiesenberg GLB, Stolnikova E et al (2014) Spatial distribution and turnover of root-derived carbon in alfalfa rhizosphere depending on top- and subsoil properties and mycorrhization. Plant Soil 380:101–115. CrossRefGoogle Scholar
  16. Haichar Z, Santaella C, Heulin T (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80. CrossRefGoogle Scholar
  17. Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–2402CrossRefGoogle Scholar
  18. Herman DJ, Johnson KK, Jaeger CH et al (2006) Root influence on nitrogen mineralization and nitrification in rhizosphere soil. Soil Sci Soc Am J 70:1504. CrossRefGoogle Scholar
  19. Holz M, Zarebanadkouki M, Kuzyakov Y et al (2017) Root hairs increase rhizosphere extension and carbon input to soil. Ann Bot.
  20. Iijima M, Griffiths B, Bengough AG (2000) Sloughing of cap cells and carbon exudation from maize seedling roots in compacted sand. New Phytol 145:477–482CrossRefGoogle Scholar
  21. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480. CrossRefGoogle Scholar
  22. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33CrossRefGoogle Scholar
  23. Kaestner A, Kühne G, Frei G, Lehmann E (2015) The ICON beamline — a facility for cold neutron imaging at SINQ. Nucl Instrum Methods Phys 659:387–393. CrossRefGoogle Scholar
  24. Kim TK, Silk WK, Cheer AY (1999) A mathematical model for pH patterns in the rhizospheres. Plant Cell Environ 22:1527–1538CrossRefGoogle Scholar
  25. Kroener E, Zarebanadkouki M, Kaestner A, Carmintati A (2014) Nonequilibrium water dynamics in the rhizosphere: how mucilage affects water flow in soils. Water Resour Res 50:6479–6495. CrossRefGoogle Scholar
  26. Kuzyakov Y, Xu X (2013) Tansley review competition between roots and microorganisms for nitrogen : mechanisms and ecological relevance. New Phytol 198:656–669CrossRefPubMedGoogle Scholar
  27. Kuzyakov Y, Raskatov A, Kaupenjohann M (2003) Turnover and distribution of root exudates of Zea Mays. Plant Soil 254:317–327CrossRefGoogle Scholar
  28. Kuzyakov Y, Shevtzova E, Pustovoytov K (2006) Carbonate re-crystallization in soil revealed by 14C labeling: experiment, model and significance for paleo-environmental reconstructions. Geoderma 131:45–58. CrossRefGoogle Scholar
  29. Landi L, Valori F, Ascher J et al (2006) Root exudate effects on the bacterial communities, CO2 evolution, nitrogen transformations and ATP content of rhizosphere and bulk soils. Soil Biol Biochem 38:509–516CrossRefGoogle Scholar
  30. McCully ME, Boyer JS (1997) The expansion of maize root-cap mucilage during hydration. 3. Changes in water potential and water content. Physiol Plant 99(1):169–177Google Scholar
  31. Meharg AA, Killham K (1995) Loss of exudates from the roots of perennial ryegrass inoculated with a range of microorganisms. Plant Soil 170:345–349CrossRefGoogle Scholar
  32. Millingtion RJ, Quirk JP (1961) Permeability of porous solids. Trans Faraday Soc 57:1200–1207CrossRefGoogle Scholar
  33. Nguyen C (2003) Rhizodeposition of organic C by plants : mechanisms and controls. Agronomie 23:375–396. CrossRefGoogle Scholar
  34. North GB, Nobel PS (1997) Drought-induced changes in soil contact and hydraulic conductivity for roots of Opuntia ficus-indica with and without rhizosheaths. Plant Soil 191:249–258. CrossRefGoogle Scholar
  35. Palta JA, Gregory PJ (1997) Drought effects the fluxes of carbon to roots and soil in 13C pulse-labelled plants of wheat. Soil Biol Biochem 29:1395–1403CrossRefGoogle Scholar
  36. Pausch J, Kuzyakov Y (2011) Photoassimilate allocation and dynamics of hotspots in roots visualized by 14C phosphor imaging. J Plant Nutr Soil Sci 174:12–19. CrossRefGoogle Scholar
  37. Personeni E, Nguyen C, Marchal P, Pages L (2007) Experimental evaluation of an efflux-influx model of C exudation by individual apical root segments. J Exp Bot 58:2091–2099. CrossRefPubMedGoogle Scholar
  38. Preece C, Penuelas J (2016) Rhizodeposition under drought and consequences for soil communities and ecosystem resilience. Plant Soil 409:1–17. CrossRefGoogle Scholar
  39. Raynaud X (2010) Soil properties are key determinants for the development of exudate gradients in a rhizosphere simulation model. Soil Biol Biochem 42:210–219. CrossRefGoogle Scholar
  40. Reid CPP, Mexal JG (1977) Water stress effects on root exudation by lodgepole pine. Soil Biol Biochem 9:417–421CrossRefGoogle Scholar
  41. Sanaullah M, Chabbi A, Rumpel C, Kuzyakov Y (2012) Soil Biology & Biochemistry C pulse labeling. Soil Biol Biochem 55:132–139. CrossRefGoogle Scholar
  42. Schweinsberg-Mickan MS, Jörgensen RG, Müller T (2012) Rhizodeposition : Its contribution to microbial growth and carbon and nitrogen turnover within the rhizosphere. J Plant Nutr Soil Sci 175:750–760. CrossRefGoogle Scholar
  43. Sharp RE, Poroyko V, Hejlek LG et al (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55:2343–2351. CrossRefPubMedGoogle Scholar
  44. Soille P (2003) Morphological image analysis: principles and applications. Spiringer Verlag, BerlinGoogle Scholar
  45. Toal ME, Yeomans C, Killham K, Meharg AA (2000) A review of rhizosphere carbon flow modelling. Plant Soil 222:263–281. CrossRefGoogle Scholar
  46. Young IM (1995) Variation in moisture contents between bulk soil and the rhizosheath of wheat (Triticum Aestivum L. cv. Wembley). New Phytol 130:135–139CrossRefGoogle Scholar
  47. Zarebanadkouki M, Kim YX, Moradi AB et al (2012) Quantification and modeling of local root water uptake using neutron radiography and deuterated water. Vadose Zone J.
  48. Zarebanadkouki M, Ahmed MA, Carminati A (2016) Hydraulic conductivity of the root-soil interface of lupin in sandy soil after drying and rewetting. Plant Soil 398:267–280. CrossRefGoogle Scholar
  49. Zhu B, Cheng W (2013) Impacts of drying - wetting cycles on rhizosphere respiration and soil organic matter decomposition. Soil Biol Biochem 63:89–96. CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  • Maire Holz
    • 1
    • 2
    Email author
  • Mohsen Zarebanadkouki
    • 2
  • Anders Kaestner
    • 3
  • Yakov Kuzyakov
    • 1
    • 4
  • Andrea Carminati
    • 2
  1. 1.Department of Agricultural Soil ScienceUniversity of GoettingenGoettingenGermany
  2. 2.Division of Soil PhysicsUniversity of BayreuthBayreuthGermany
  3. 3.Paul Scherrer InstiuteVilligenSwitzerland
  4. 4.Institute of Environmental SciencesKazan Federal UniversityKazanRussia

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