Effects of soil nitrogen availability on rhizodeposition in plants: a review

Bowsher, Alan W.; Evans, Sarah; Tiemann, Lisa K.; Friesen, Maren L.

doi:10.1007/s11104-017-3497-1

Effects of soil nitrogen availability on rhizodeposition in plants: a review

Regular Article
Published: 20 November 2017

Volume 423, pages 59–85, (2018)
Cite this article

Plant and Soil Aims and scope Submit manuscript

Alan W. Bowsher¹,
Sarah Evans²,
Lisa K. Tiemann³ &
…
Maren L. Friesen^1,4

2815 Accesses
43 Citations
4 Altmetric
Explore all metrics

Abstract

Background

Soil contains the majority of terrestrial carbon (C), forming the foundation for soil fertility and nutrient cycling. One key source of soil C is root-derived C, or rhizodeposits, which signal and sustain microbes that cycle nutrients such as nitrogen (N). Although N availability can affect rhizodeposition both quantitatively and qualitatively, these effects remain poorly understood due to conflicting results among studies.

Scope

Here, we review studies examining the influence of soil N availability on rhizodeposition. We conduct a quantitative analysis of the response of various rhizodeposition C pools to N availability, and assess methodological aspects potentially underlying the highly variable results among studies. We also review impacts of N availability on the composition and quality of rhizodeposits.

Conclusions

Effects of N on rhizodeposition were strongly dependent upon the specific C pools considered and the units for reporting those pools. N additions increased nearly all rhizodeposit C pools when expressed on a per plant basis, and decreased rhizodeposition per unit fixed C for several C pools, while no rhizodeposition C pools were significantly altered when expressed per unit root mass. Nevertheless, N effects were generally mixed due to a combination of variation in experimental methods and species-specific responses. Overall, our review indicates several key challenges for better understanding the mechanistic links between N availability, plant physiology, and microbial function. Identifying such links would substantially improve our ability to predict C- and N-dynamics in changing ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

The rhizosphere effect on soil gross nitrogen mineralization: A meta-analysis

Article 15 June 2021

Rhizodeposition of organic carbon by plants with contrasting traits for resource acquisition: responses to different fertility regimes

Article 07 June 2015

Rhizodeposition under drought and consequences for soil communities and ecosystem resilience

Article 10 November 2016

References

Aitkenhead-Peterson JA, Kalbitz K (2005) Short-term response on the quantity and quality of rhizo-deposited carbon from Norway spruce exposed to low and high N inputs. J Plant Nutr Soil Sci 168:687–693. https://doi.org/10.1002/jpln.200420468
Article CAS Google Scholar
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827. https://doi.org/10.1038/nature03608
Article CAS PubMed Google Scholar
Allard V, Robin C, Newton PCD et al (2006) Short and long-term effects of elevated CO₂ on Lolium perenne rhizodeposition and its consequences on soil organic matter turnover and plant N yield. Soil Biol Biochem 38:1178–1187. https://doi.org/10.1016/j.soilbio.2005.10.002
Article CAS Google Scholar
Atere CT, Ge T, Zhu Z et al (2017) Rice rhizodeposition and carbon stabilisation in paddy soil are regulated via drying-rewetting cycles and nitrogen fertilisation. Biol Fertil Soils 53:407–417. https://doi.org/10.1007/s00374-017-1190-4
Article CAS Google Scholar
Balesdent J, Balabane M (1992) Maize root-derived soil organic-carbon estimated by natural ¹³C abundance. Soil Biol Biochem 24:97–101. https://doi.org/10.1016/0038-0717(92)90264-x
Article Google Scholar
Balesdent J, Mariotti A, Guillet B (1987) Natural ¹³C abundance as a tracer for studies of soil organic matter dynamics. Soil Biol Biochem 19:25–30. https://doi.org/10.1016/0038-0717(87)90120-9
Article CAS Google Scholar
Baptist F, Aranjuelo I, Legay N et al (2015) Rhizodeposition of organic carbon by plants with contrasting traits for resource acquisition: responses to different fertility regimes. Plant Soil 394:391–406. https://doi.org/10.1007/s11104-015-2531-4
Article CAS Google Scholar
Bazot S, Ulff L, Blum H et al (2006) Effects of elevated CO₂ concentration on rhizodeposition from Lolium perenne grown on soil exposed to 9 years of CO₂ enrichment. Soil Biol Biochem 38:729–736. https://doi.org/10.1016/j.soilbio.2005.06.023
Article CAS Google Scholar
Besserer A, Puech-Pagès V, Kiefer P et al (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:1239–1247. https://doi.org/10.1371/journal.pbio.0040226
Article CAS Google Scholar
Billes G, Rouhier H, Bottner P (1993) Modifications of the carbon and nitrogen allocations in the plant (Triticum aestivum L.) soil system in response to increased atmospheric CO₂ concentration. Plant Soil 157:215–225
Article CAS Google Scholar
Bingeman CW, Varner JE, Martin WP (1953) The effect of the addition of organic materials on the decomposition of an organic soil. Soil Sci Soc Am Proc 17:34–38. https://doi.org/10.2136/sssaj1953.03615995001700010008x
Article CAS Google Scholar
Biondini M, Klein DA, Redente EF (1988) Carbon and nitrogen losses through root exudation by Agropyron cristatum, Agropyron smithii and Bouteloua gracilis. Soil Biol Biochem 20:477–482. https://doi.org/10.1016/0038-0717(88)90061-2
Article Google Scholar
Blagodatskaya E, Blagodatsky S, Dorodnikov M, Kuzyakov Y (2010) Elevated atmospheric CO₂ increases microbial growth rates in soil: results of three CO₂ enrichment experiments. Glob Chang Biol 16:836–848. https://doi.org/10.1111/j.1365-2486.2009.02006.x
Article Google Scholar
Bowen GD (1969) Nutrient status effects on loss of amides and amino acids from pine roots. Plant Soil 30:139–142
Article CAS Google Scholar
Bradford MA, Fierer N, Jackson RB et al (2008) Nonlinear root-derived carbon sequestration across a gradient of nitrogen and phosphorous deposition in experimental mesocosms. Glob Chang Biol 14:1113–1124. https://doi.org/10.1111/j.1365-2486.2008.01564.x
Article Google Scholar
Bremer E, van Kessel C (1990) Extractability of microbial ¹⁴C and ¹⁵N following addition of variable rates of labelled glucose and (NH₄)₂SO₄ to soil. Soil Biol Biochem 22:707–713. https://doi.org/10.1016/0038-0717(90)90019-V
Article CAS Google Scholar
Bringhurst RM, Cardon ZG, Gage DJ (2001) Galactosides in the rhizosphere: utilization by Sinorhizobium meliloti and development of a biosensor. Proc Natl Acad Sci U S A 98:4540–4545. https://doi.org/10.1073/pnas.071375898
Article CAS PubMed PubMed Central Google Scholar
Bürgmann H, Meier S, Bunge M et al (2005) Effects of model root exudates on structure and activity of a soil diazotroph community. Environ Microbiol 7:1711–1724. https://doi.org/10.1111/j.1462-2920.2005.00818.x
Article PubMed CAS Google Scholar
Bushby HVA, Vallis I, Myers RJK (1992) Dynamics of C in a pasture grass (Panicum maximum Var. Trichoglume)-soil system. Soil Biol Biochem 24:381–387. https://doi.org/10.1016/0038-0717(92)90198-7
Article Google Scholar
Butterly CR, Armstrong R, Chen D, Tang C (2015) Carbon and nitrogen partitioning of wheat and field pea grown with two nitrogen levels under elevated CO₂. Plant Soil 391:367–382. https://doi.org/10.1007/s11104-015-2441-5
Article CAS Google Scholar
Cakmak I, Marschner H (1988) Increase in membrane permeability and exudation in roots of zinc deficient plants. J Plant Physiol 132:356–361
Article CAS Google Scholar
Carvalhais LC, Dennis PG, Fedoseyenko D et al (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. https://doi.org/10.1002/jpln.201000085
Article CAS Google Scholar
Cerri C, Feller C, Balesdent J et al (1985) Application du traçage isotopique naturel en ¹³C, à l’étude de la dynamique de la matière organique dans les sols. Comptes Rendus l’Académie des Sci des Paris 300:423–427
Google Scholar
Chapin FS III, Schulze E-D, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Evol Syst 21:423–447
Article Google Scholar
Cheng W (1996) Measurement of rhizosphere respiration and organic matter decomposition using natural ¹³C. Plant Soil 183:263–268. https://doi.org/10.1007/BF00011441
Article CAS Google Scholar
Cheng W, Johnson DW (1998) Elevated CO₂, rhizosphere processes, and soil organic matter decomposition. Plant Soil 202:167–174
Article CAS Google Scholar
Cheng W, Parton WJ, Gonzalez-Meler MA et al (2014) Synthesis and modeling perspectives of rhizosphere priming. New Phytol 201:31–44
Article CAS PubMed Google Scholar
Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17:181–187. https://doi.org/10.1016/0038-0717(85)90113-0
Article CAS Google Scholar
Cotrufo MF, Gorissen A (1997) Elevated CO₂ enhances below-ground C allocation in three perennial grass species at different levels of N availability. New Phytol 137:421–431
Article CAS Google Scholar
Dakora FD, Joseph CM, Phillips DA (1993) Alfalfa (Medicago sativa 1.) root exudates contain isoflavonoids in the presence of Rhizobium meliloti. Plant Physiol 101:819–824
Article CAS PubMed PubMed Central Google Scholar
Darwent MJ, Paterson E, McDonald AJS, Tomos AD (2003) Biosensor reporting of root exudation from Hordeum vulgare in relation to shoot nitrate concentration. J Exp Bot 54:325–334. https://doi.org/10.1093/jxb/54.381.325
Article CAS PubMed Google Scholar
Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:1–8. https://doi.org/10.3389/fmicb.2013.00216
Article CAS Google Scholar
Drake JE, Darby BA, Giasson M-A et al (2013) Stoichiometry constrains microbial response to root exudation- insights from a model and a field experiment in a temperate forest. Biogeosciences 10:821–838. https://doi.org/10.5194/bg-10-821-2013
Article CAS Google Scholar
Falkengren-Grerup U (1995) Interspecies differences in the preference of ammonium and nitrate in vascular plants. Oecologia 102:305–311. https://doi.org/10.1007/bf00329797
Article PubMed Google Scholar
Farrar JF, Jones DL (2000) The control of carbon acquisition by roots. New Phytol 147:43–53. https://doi.org/10.1046/j.1469-8137.2000.00688.x
Article CAS Google Scholar
Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84:827–837
Article Google Scholar
Fernandez I, Cadisch G (2003) Discrimination against ¹³C during degradation of simple and complex substrates by two white rot fungi. Rapid Commun Mass Spectrom 17:2614–2620. https://doi.org/10.1002/rcm.1234
Article CAS PubMed Google Scholar
Fierer N, Lauber CL, Ramirez KS et al (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017. https://doi.org/10.1038/ismej.2011.159
Article CAS PubMed Google Scholar
Finzi AC, Abramoff RZ, Spiller KS et al (2015) Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob Chang Biol 21:2082–2094. https://doi.org/10.1111/gcb.12816
Article PubMed Google Scholar
Fog K (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63:433–462
Article Google Scholar
Fontaine S, Bardoux G, Abbadie L, Mariotti A (2004) Carbon input to soil may decrease soil carbon content. Ecol Lett 7:314–320. https://doi.org/10.1111/j.1461-0248.2004.00579.x
Article Google Scholar
Fox J, Weisberg S (2011) An {R} Companion to Applied Regression, Second Edition. Thousand Oaks CA: Sage. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion
Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171. https://doi.org/10.1016/j.foreco.2004.03.018
Article Google Scholar
Gavrichkova O, Kuzyakov Y (2008) Ammonium versus nitrate nutrition of Zea mays and Lupinus albus: effect on root-derived CO₂ efflux. Soil Biol Biochem 40:2835–2842. https://doi.org/10.1016/j.soilbio.2008.08.003
Article CAS Google Scholar
Gavrichkova O, Kuzyakov Y (2010) Respiration costs associated with nitrate reduction as estimated by ¹⁴CO₂ pulse labeling of corn at various growth stages. Plant Soil 329:433–445. https://doi.org/10.1007/s11104-009-0169-9
Article CAS Google Scholar
Ge T, Liu C, Yuan H et al (2015) Tracking the photosynthesized carbon input into soil organic carbon pools in a rice soil fertilized with nitrogen. Plant Soil 392:17–25. https://doi.org/10.1007/s11104-014-2265-8
Article CAS Google Scholar
Ge T, Li B, Zhu Z et al (2017) Rice rhizodeposition and its utilization by microbial groups depends on N fertilization. Biol Fertil Soils 53:37–48. https://doi.org/10.1007/s00374-016-1155-z
Article CAS Google Scholar
Geddes BA, Ryu M-H, Mus F et al (2015) Use of plant colonizing bacteria as chassis for transfer of N₂-fixation to cereals. Curr Opin Biotechnol 32:216–222. https://doi.org/10.1016/j.copbio.2015.01.004
Article CAS PubMed Google Scholar
Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms - a review. Soil Biol Biochem 75:54–63. https://doi.org/10.1016/j.soilbio.2014.03.023
Article CAS Google Scholar
Geisseler D, Lazicki PA, Scow KM (2016) Mineral nitrogen input decreases microbial biomass in soils under grasslands but not annual crops. Appl Soil Ecol 106:1–10. https://doi.org/10.1016/j.apsoil.2016.04.015
Article Google Scholar
Gillespie IMM, Deacon JW (1988) Effects of mineral nutrients on senescence of the cortex of wheat roots and root pieces. Soil Biol Biochem 20:525–531
Article CAS Google Scholar
van Ginkel JH, Gorissen A (1998) In situ decomposition of grass roots as affected by elevated atmospheric carbon dioxide. Soil Sci Soc Am J 62:951–958
Article Google Scholar
van Ginkel JH, Gorissen A, van Veen JA (1997) Carbon and nitrogen allocation in Lolium perenne in response to elevated atmospheric CO₂ with emphasis on soil carbon dynamics. Plant Soil 188:299–308. https://doi.org/10.1023/A:1004233920896
Article Google Scholar
Glanville HC, Hill PW, Schnepf A et al (2016) Combined use of empirical data and mathematical modelling to better estimate the microbial turnover of isotopically labelled carbon substrates in soil. Soil Biol Biochem 94:154–168. https://doi.org/10.1016/j.soilbio.2015.11.016
Article CAS Google Scholar
Gorissen A, van Ginkel JH, van de Beek H (1995) Carbon allocation in mature grass (Lolium perenne) under elevated CO₂ at two soil nitrogen levels. In: Zwerver S, van Rompaey RSAR, Kok MTJ, Berk MM (eds) studies in environmental science 65B: climate change research evaluation and policy implications. Elsevier science B.V., Amsterdam, the Netherlands, pp 735–740
de Graaff M-A, Six J, van Kessel C (2007) Elevated CO₂ increases nitrogen rhizodeposition and microbial immobilization of root-derived nitrogen. New Phytol 173:778–786. https://doi.org/10.1111/j.1469-8137.2006.01974.x
Article PubMed CAS Google Scholar
de Graaff M, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188:1055–1064. https://doi.org/10.1111/j.1469-8137.2010.03427.x
Article PubMed CAS Google Scholar
de Graaff M-A, Jastrow JD, Gillette S et al (2014) Differential priming of soil carbon driven by soil depth and root impacts on carbon availability. Soil Biol Biochem 69:147–156. https://doi.org/10.1016/j.soilbio.2013.10.047
Article CAS Google Scholar
Graham JH, Leonard RT, Menge JA (1981) Membrane-mediated decrease in root exudation responsible for phosphorus inhibition of vesicular-arbuscular mycorrhiza formation. Plant Physiol 68:548–552
Article CAS PubMed PubMed Central Google Scholar
Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56. https://doi.org/10.1016/s0929-1393(96)00126-6
Article Google Scholar
Gregorich EG, Ellert BH, Drury CF, Liang BC (1996) Fertilization effects on soil organic matter turnover and corn residue C storage. Soil Sci Soc Am J 60:472–476
Article CAS Google Scholar
Gschwendtner S, Engel M, Lueders T et al (2016) Nitrogen fertilization affects bacteria utilizing plant-derived carbon in the rhizosphere of beech seedlings. Plant Soil 407:203–215. https://doi.org/10.1007/s11104-016-2888-z
Article CAS Google Scholar
Halvorson AD, Reule CA, Follett RF (1999) Nitrogen fertilization effects on soil carbon and nitrogen in a dryland cropping system. Soil Sci Soc Am J 63:912–917
Article CAS Google Scholar
Halvorson AD, Wienhold BJ, Black AL (2002) Tillage, nitrogen, and cropping system effects on soil carbon sequestration. Soil Sci Soc Am J 66:906–912. https://doi.org/10.2136/sssaj2002.0906
Article CAS Google Scholar
Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–146. https://doi.org/10.1023/A:1006244819642
Article CAS Google Scholar
Henry F, Nguyen C, Paterson E, et al (2005) How does nitrogen availability alter rhizodeposition in Lolium multiflorum lam. During vegetative growth? In: plant and soil. Pp 181–191
Hill PW, Marshall C, Williams GG et al (2007) The fate of photosynthetically-fixed carbon in Lolium perenne grassland as modified by elevated CO₂ and sward management. New Phytol 173:766–777. https://doi.org/10.1111/j.1469-8137.2006.01966.x
Article CAS PubMed Google Scholar
Hobbie SE (2000) Interactions between litter lignin and soil nitrogen availability during leaf litter decomposition in a hawaiian montane forest. Ecosystems 3:484–494. https://doi.org/10.1007/s100210000042
Article CAS Google Scholar
Hodge A, Grayston SJ, Ord BG (1996) A novel method for characterisation and quantification of plant root exudates. Plant Soil 184:97–104
Hoosbeek MR, Li Y, Scarascia-Mugnozza GE (2006) Free atmospheric CO₂ enrichment (FACE) increased labile and total carbon in the mineral soil of a short rotation Poplar plantation. Plant Soil 281:247–254. https://doi.org/10.1007/s11104-005-4293-x
Article CAS Google Scholar
Hopkins F, Gonzalez-Meler MA, Flower CE et al (2013) Ecosystem-level controls on root-rhizosphere respiration. New Phytol 199:339–351
Article CAS PubMed Google Scholar
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
Indorf C, Dyckmans J, Joergensen RG (2015) Short-term changes in amino sugar-specific δ¹³C values after application of C₄ and C₃ sucrose. Soil Biol Biochem 91:92–98. https://doi.org/10.1016/j.soilbio.2015.08.028
Article CAS Google Scholar
IPCC (2014) Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change [Core writing team, R.K. Pachauri and L.a. Meyer (eds.)]. IPCC, Geneva, Switzerland, 151 pp.
Jackson LE, Burger M, Cavagnaro TR (2008) Roots, nitrogen transformations, and ecosystem services. Annu Rev Plant Biol 59:341–363. https://doi.org/10.1146/annurev.arplant.59.032607.092932
Article CAS PubMed Google Scholar
Jaeger CHI, Lindow SE, Miller W et al (1999) Mapping sugar and amino availability in soil around roots using bacterial sensors of sucrose and tryptophan. Appl Environ Microbiol 65:2685–2690
CAS PubMed PubMed Central Google Scholar
Jensen B, Christensen BT (2004) Interactions between elevated CO₂ and added N: effects on water use, biomass, and soil N-15 uptake in wheat. Acta Agric Scand Sect B-Soil Plant Sci 54:175–184. https://doi.org/10.1080/09064710410035613
CAS Google Scholar
Johansson G (1992) Below-ground carbon distribution in barley (Hordeum vulgare L.) with and without nitrogen fertilization. Plant Soil 144:93–99
Article CAS Google Scholar
Jones DL, Darrah PR (1994) Amino-acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere. Plant Soil 163:1–12
Article CAS Google Scholar
Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33. https://doi.org/10.1007/s11104-009-9925-0
Article CAS Google Scholar
Kanakidou M, Myriokefalitakis S, Daskalakis N et al (2016) Past, present and future atmospheric nitrogen deposition. J Atmos Sci 73:2039–2047. https://doi.org/10.1175/JAS-D-15-0278.1
Article Google Scholar
Kanders MJ, Berendonk C, Fritz C et al (2017) Catch crops store more nitrogen below-ground when considering rhizodeposits. Plant Soil:1–13. https://doi.org/10.1007/s11104-017-3259-0
Kell DB (2012) Large-scale sequestration of atmospheric carbon via plant roots in natural and agricultural ecosystems: why and how. Philos Trans R Soc B Biol Sci 367:1589–1597. https://doi.org/10.1098/rstb.2011.0244
Article CAS Google Scholar
Khan SA, Mulvaney RL, Ellsworth TR, Boast CW (2007) The myth of nitrogen fertilization for soil carbon sequestration. J Environ Qual 36:1821–1832. https://doi.org/10.2134/jeq2007.0099
Article CAS PubMed Google Scholar
Kiba T, Krapp A (2016) Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant Cell Physiol 57:707–714. https://doi.org/10.1093/pcp/pcw052
Article CAS PubMed PubMed Central Google Scholar
Kraiser T, Gras DE, Gutiérrez AG et al (2011) A holistic view of nitrogen acquisition in plants. J Exp Bot 62:1455–1466. https://doi.org/10.1093/jxb/erq425
Article CAS PubMed PubMed Central Google Scholar
Kretzschmar T, Kohlen W, Sasse J et al (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344
Article CAS PubMed Google Scholar
van der Krift TAJ, Kuikman PJ, Möller F, Berendse F (2001) Plant species and nutritional-mediated control over rhizodeposition and root decomposition. Plant Soil 228:191–200. https://doi.org/10.1023/A:1004834128220
Article Google Scholar
Kuijken RCP, Snel JFH, Heddes MM et al (2015) The importance of a sterile rhizosphere when phenotyping for root exudation. Plant Soil 387:131–142. https://doi.org/10.1007/s11104-014-2283-6
Article CAS Google Scholar
Kuzyakov Y (2002a) Separating microbial respiration of exudates from root respiration in non-sterile soils: a comparison of four methods. Soil Biol Biochem 34:1621–1631
Article CAS Google Scholar
Kuzyakov Y (2002b) Review : factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci 165:382–396
Article CAS Google Scholar
Kuzyakov Y (2006) Sources of CO₂ efflux from soil and review of partitioning methods. Soil Biol Biochem 38:425–448. https://doi.org/10.1016/j.soilbio.2005.08.020
Article CAS Google Scholar
Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371. https://doi.org/10.1016/j.soilbio.2010.04.003
Article CAS Google Scholar
Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review J Plant Nutr Soil Sci 163:421–431. https://doi.org/10.1002/1522-2624(200008)163:4<421::aid-jpln421>3.0.co;2-r
Article CAS Google Scholar
Kuzyakov Y, Larionova AA (2005) Root and rhizomicrobial respiration: a review of approaches to estimate respiration by autotrophic and heterotrophic organisms in soil. J Plant Nutr Soil Sci 168:503–520. https://doi.org/10.1002/jpln.200421703
Article CAS Google Scholar
Kuzyakov Y, Schneckenberger K (2004) Review of estimation of plant rhizodeposition and their contribution to soil organic matter formation. Arch Agron Soil Sci 50:115–132. https://doi.org/10.1080/03650340310001627658
Article Google Scholar
Kuzyakov Y, Siniakina SV (2001) A novel method for separating root-derived organic compounds from root respiration in non-sterilized soils. J Plant Nutr Soil Sci 164:511–517
Article CAS Google Scholar
Kuzyakov Y, Kretzschmar A, Stahr K (1999) Contribution of Lolium perenne rhizodeposition to carbon turnover of pasture soil. Plant Soil 213:127–136
Article CAS Google Scholar
Kuzyakov Y, Biryukova O, Kuznetzova T et al (2002a) Carbon partitioning in plant and soil, carbon dioxide fluxes and enzyme activities as affected by cutting ryegrass. Biol Fertil Soils 35:348–358. https://doi.org/10.1007/s00374-002-0480-6
Article CAS Google Scholar
Kuzyakov Y, Siniakina SV, Ruehlmann J et al (2002b) Effect of nitrogen fertilisation on below-ground carbon allocation in lettuce. J Sci Food Agric 82:1432–1441. https://doi.org/10.1002/jsfa.1202
Article CAS Google Scholar
Lebauer DS, Treseder KK (2014) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379
Article Google Scholar
Lee KJ, Gaskins MH (1982) Increased root exudation of ¹⁴C-compounds by sorghum seedlings inoculated with nitrogen-fixing bacteria. Plant Soil 69:391–399
Article CAS Google Scholar
Lesuffleur F, Cliquet J-B (2010) Characterisation of root amino acid exudation in white clover (Trifolium repens L.) Plant Soil 333:191–201. https://doi.org/10.1007/s11104-010-0334-1
Article CAS Google Scholar
Levene H (1960) Robust tests for equality of variances. In: Olkin I, Ghurye S, Hoeffding W et al (eds) Contributions to probability and statistics: essays in honor of Harold Hotelling. Stanford University Press, Palo Alto, CA, USA, pp 278–292
Google Scholar
Li Y, Wang J, Pan F et al (2016) Soil nitrogen availability alters rhizodeposition carbon flux into the soil microbial community. J Soils Sediments 16:1472–1480. https://doi.org/10.1007/s11368-015-1337-6
Article CAS Google Scholar
Liljeroth E, Van Veen JA, Miller HJ (1990) Assimilate translocation to the rhizosphere of two wheat lines and subsequent utilization by rhizosphere microorganisms at two soil nitrogen concentrations. Soil Biol Biochem 22:1015–1021. https://doi.org/10.1016/0038-0717(90)90026-V
Article CAS Google Scholar
Liljeroth E, Kuikman P, Van Veen JA (1994) Carbon translocation to the rhizosphere of maize and wheat and influence on the turnover of native soil organic matter at different soil nitrogen levels. Plant Soil 161:233–240. https://doi.org/10.1007/BF00046394
Article Google Scholar
Lloyd DA, Ritz K, Paterson E, Kirk GJ (2016) Effects of soil type and composition of rhizodeposits on rhizosphere priming phenomena. Soil Biol Biochem 103:512–521. https://doi.org/10.1016/j.soilbio.2016.10.002
Article CAS Google Scholar
Lodhi A, Sajjad MH, Mahmood A et al (2009) Photosynthate partitioning in wheat (Triticum aestivum L.) as affected by root-zone salinity and form of N. Pakistan J Bot 41:1363–1372. https://doi.org/10.1007/s11738-008-0191-1
CAS Google Scholar
Lv F, Xue S, Wang G, Zhang C (2017) Nitrogen addition shifts the microbial community in the rhizosphere of Pinus tabuliformis in northwestern China. PLoS One:1–14. https://doi.org/10.1371/journal.pone.0172382
Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10. https://doi.org/10.1007/BF00011685
Article CAS Google Scholar
Maaroufi NI, Nordin A, Hasselquist NJ et al (2015) Anthropogenic nitrogen deposition enhances carbon sequestration in boreal soils. Glob Chang Biol 21:3169–3180. https://doi.org/10.1111/gcb.12904
Article PubMed Google Scholar
McDougall BM, Rovira AD (1970) Sites of exudation of ¹⁴C-labelled compounds from wheat roots. New Phytol 69:999–1003
Article Google Scholar
Meharg AA (1994) A critical review of labelling techniques used to quantify rhizosphere carbon-flow. Plant Soil 166:55–62
Article CAS Google Scholar
Meharg AA, Killham K (1988) A comparison of carbon flow from pre-labelled and pulse-labelled plants. Plant Soil 112:225–231. https://doi.org/10.1007/BF02139999
Article Google Scholar
Meier IC, Finzi AC, Phillips RP (2017) Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools. Soil Biol Biochem 106:119–128. https://doi.org/10.1016/j.soilbio.2016.12.004
Article CAS Google Scholar
Mikan CJ, Zak DR, Kubiske ME, Pregitzer KS (2000) Combined effects of atmospheric CO₂ and N availability on the belowground carbon and nitrogen dynamics of aspen mesocosms. Oecologia 124:432–445. https://doi.org/10.1007/PL00008869
Article CAS PubMed Google Scholar
Mühling KH, Schubert S, Mengel K (1993) Role of plasmalemma H+ATPase in sugar retention by roots of intact maize and field bean plants. J Plant Nutr Soil Sci 156:155–161
Google Scholar
Mus F, Crook MB, Garcia K et al (2016) Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl Environ Microbiol 82:3698–3710. https://doi.org/10.1128/AEM.01055-16
Article CAS PubMed PubMed Central Google Scholar
Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29. https://doi.org/10.1007/s11104-013-1645-9
Article CAS Google Scholar
Neff JC, Townsend AR, Gleixner G et al (2002) Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419:915–917. https://doi.org/10.1038/Nature01136
Article CAS PubMed Google Scholar
Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. In: Agronomie, pp 375–396
Google Scholar
Nie M, Lu M, Bell J et al (2013) Altered root traits due to elevated CO₂: a meta-analysis. Glob Ecol Biogeogr 22:1095–1105. https://doi.org/10.1111/geb.12062
Article Google Scholar
O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336
Article Google Scholar
Paterson E (2003) Importance of rhizodeposition in the coupling of plant and microbial productivity. Eur J Soil Sci 54:741–750. https://doi.org/10.1046/j.1351-0754.2003.0557.x
Article Google Scholar
Paterson E, Sim A (1999) Rhizodeposition and C-partitioning of Lolium perenne in axenic culture affected by nitrogen supply and defoliation. Plant Soil 216:155–164. https://doi.org/10.1023/a:1004789407065
Article CAS Google Scholar
Paterson E, Sim A (2000) Effect of nitrogen supply and defoliation on loss of organic compounds from roots of Festuca rubra. J Exp Bot 51:1449–1457. https://doi.org/10.1093/jexbot/51.349.1449
Article CAS PubMed Google Scholar
Paterson E, Hall JM, Rattray EAS et al (1997) Effect of elevated CO₂ on rhizosphere carbon flow and soil microbial processes. Glob Chang Biol 3:363–377. https://doi.org/10.1046/j.1365-2486.1997.t01-1-00088.x
Article Google Scholar
Pausch J, Tian J, Riederer M, Kuzyakov Y (2013) Estimation of rhizodeposition at field scale: upscaling of a ¹⁴C labeling study. Plant Soil 364:273–285. https://doi.org/10.1007/s11104-012-1363-8
Article CAS Google Scholar
Phillips RP, Bernhardt ES, Schlesinger WH (2009) Elevated CO₂ increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response. Tree Physiol 29:1513–1523. https://doi.org/10.1093/treephys/tpp083
Article CAS PubMed Google Scholar
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. https://doi.org/10.1111/j.1461-0248.2010.01570.x
Article PubMed Google Scholar
Pii Y, Mimmo T, Tomasi N et al (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol Fertil Soils 51:403–415. https://doi.org/10.1007/s00374-015-0996-1
Article CAS Google Scholar
Poorter H, Niklas KJ, Reich PB et al (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50
Article CAS PubMed Google Scholar
Qian JH, Doran JW, Walters DT (1997) Maize plant contributions to root zone available carbon and microbial transformations of nitrogen. Soil Biol Biochem 29:1451–1462
Article CAS Google Scholar
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Radajewski S, Ineson P, Parekh NR, Murrell JC (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403:646–649. https://doi.org/10.1038/35001054
Article CAS PubMed Google Scholar
Rasse DP, Rumpel C, Dignac M-F (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356. https://doi.org/10.1007/s11104-004-0907-y
Article CAS Google Scholar
Remans T, Nacry P, Pervent M et al (2006) A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiol 140:909–921. https://doi.org/10.1104/pp.105.075721
Article CAS PubMed PubMed Central Google Scholar
Robinson D, Rorison IH (1987) Root hairs and plant growth at low nitrogen availabilities. New Phytol 107:681–693
Article Google Scholar
Robinson D, Griffiths B, Ritz K, Wheatley R (1989) Root-induced nitrogen mineralisation: a theoretical analysis. Plant Soil 117:185–193
Article CAS Google Scholar
Rovira A (1965) Interactions between plant roots and soil microorganisms. Annu Rev Microbiol 19:241–266
Article CAS PubMed Google Scholar
Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556. https://doi.org/10.1104/pp.108.127613
Article CAS PubMed PubMed Central Google Scholar
Saggar S, Hedley C, Mackay AD (1997) Partitioning and translocation of photosynthetically fixed ¹⁴C in grazed hill pastures. Biol Fertil Soils 25:152–158
Article Google Scholar
Sapronov DV, Kuzyakov YV (2007) Separation of root and microbial respiration: comparison of three methods. Eurasian Soil Sci 40:775–784. https://doi.org/10.1134/S1064229307070101
Article Google Scholar
Schenck Zu Schweinsberg-Mickan M, 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. https://doi.org/10.1002/jpln.201100300
Article CAS Google Scholar
Schimel DS (1995) Terrestrial ecosystems and the carbon cycle. Glob Chang Biol 1:77–91
Article Google Scholar
Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20
Article CAS Google Scholar
Schuur EAG, Trumbore SE (2006) Partitioning sources of soil respiration in boreal black spruce forest using radiocarbon. Glob Chang Biol 12:165–176
Article Google Scholar
Shamoot S, McDonald L, Bartholomew WV (1968) Rhizo-deposition of organic debris in soils. Soil Sci Soc Am Proc 32:817–820
Article CAS Google Scholar
Singh BK, Millard P, Whiteley AS, Murrell JC (2004) Unravelling rhizosphere-microbial interactions: opportunities and limitations. Trends Microbiol 12:386–393. https://doi.org/10.1016/j.tim.2004.06.008
Article CAS PubMed Google Scholar
Snedecor G, Cochran W (1989) Statistical methods. Iowa State University Press, Ames, IA, USA, Eight
Google Scholar
Swinnen J (1994) Evaluation of the use of a model rhizodeposition technique to separate root and microbial respiration in soil. Plant Soil 165:89–101
Article CAS Google Scholar
Tiemann LK, Billings SA (2011) Indirect effects of nitrogen amendments on organic substrate quality increase enzymatic activity driving decomposition in a mesic grassland. Ecosystems 14:234–247. https://doi.org/10.1007/s10021-010-9406-6
Article CAS Google Scholar
Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120
Article PubMed Google Scholar
Uren N (2001) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere – biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 19–40
Google Scholar
Uselman SM, Qualls RG, Thomas RB (2000) Effects of increased atmospheric CO₂, temperature, and soil N availability on root exudation of dissolved organic carbon by a N-fixing tree (Robinia pseudoacacia L.) Plant Soil 222:191–202. https://doi.org/10.1023/A:1004705416108
Article CAS Google Scholar
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707
Article CAS Google Scholar
van Veen JA, Liljeroth E, Lekkerkerk LJA, van de Geijn SC (1991) Carbon fluxes in plant-soil systems at elevated atmospheric CO₂ levels. Ecol Appl 1:175–181
Article PubMed Google Scholar
Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115
Article Google Scholar
Vitousek PM, Aber JD, Howarth RW et al (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750
Google Scholar
Vranova V, Rejsek K, Skene KR et al (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. https://doi.org/10.1002/jpln.201000360
Article CAS Google Scholar
van der Wal A, de Boer W (2017) Dinner in the dark: illuminating drivers of soil organic matter decomposition. Soil Biol Biochem 105:45–48. https://doi.org/10.1016/j.soilbio.2016.11.006
Article CAS Google Scholar
Wang J, Chapman SJ, Yao H (2016) Incorporation of ¹³C-labelled rice rhizodeposition into soil microbial communities under different fertilizer applications. Appl Soil Ecol 101:11–19. https://doi.org/10.1016/j.apsoil.2016.01.010
Article Google Scholar
Werth M, Kuzyakov Y (2010) ¹³C fractionation at the root-microorganisms-soil interface: a review and outlook for partitioning studies. Soil Biol Biochem 42:1372–1384. https://doi.org/10.1016/j.soilbio.2010.04.009
Article CAS Google Scholar
Whipps JM, Lynch JM (1983) Substrate flow and utilization in the rhizosphere of cereals. New Phytol 95:605–623
Article CAS Google Scholar
Wichern F, Eberhardt E, Mayer J et al (2008) Nitrogen rhizodeposition in agricultural crops: methods, estimates and future prospects. Soil Biol Biochem 40:30–48. https://doi.org/10.1016/j.soilbio.2007.08.010
Article CAS Google Scholar
von Wirén N, Lauter F-R, Ninnemann O et al (2000) Differential regulation of three functional ammonium transporter genes by nitrogen in root hairs and by light in leaves of tomato. Plant J 21:167–175. https://doi.org/10.1046/j.1365-313X.2000.00665.x
Article Google Scholar
Xu JG, Juma NG (1994) Relations of shoot C, root C and root length with root-released C of two barley cultivars and the decomposition of root-released C in soil. Can J Soil Sci 74:17–22
Article Google Scholar
Yin H, Li Y, Xiao J et al (2013) Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Glob Chang Biol 19:2158–2167. https://doi.org/10.1111/gcb.12161
Article PubMed Google Scholar
Yoneyama K, Xie X, Kusumoto D et al (2007a) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132. https://doi.org/10.1007/s00425-007-0600-5
Article CAS PubMed Google Scholar
Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007b) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225:1031–1038. https://doi.org/10.1007/s00425-006-0410-1
Article CAS PubMed Google Scholar
Yoneyama K, Xie X, Il KH et al (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235:1197–1207. https://doi.org/10.1007/s00425-011-1568-8
Article CAS PubMed Google Scholar
Yuan J, Zhang N, Huang Q et al (2015) Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Nat Sci Reports 5:13438. https://doi.org/10.1038/srep13438
CAS Google Scholar
Zagal E, Bjarnason S, Olsson U (1993) Carbon and nitrogen in the root-zone of barley (Hordeum vulgare L.) supplied with nitrogen fertilizer at two rates. Plant Soil 157:51–63
Article Google Scholar
el Zahar Haichar F, Marol C, Berge O et al (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230. https://doi.org/10.1038/ismej.2008.80
Article CAS Google Scholar
Zhang N, Wang D, Liu Y et al (2014) Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374:689–700. https://doi.org/10.1007/s11104-013-1915-6
Article CAS Google Scholar
Zhang K, Chen L, Li Y et al (2017) The effects of combinations of biochar, lime, and organic fertilizer on nitrification and nitrifiers. Biol Fertil Soils 53:77–87. https://doi.org/10.1007/s00374-016-1154-0
Article CAS Google Scholar
Zhu B, Cheng W (2011) ¹³C isotope fractionation during rhizosphere respiration of C₃ and C₄ plants. Plant Soil 342:277–287. https://doi.org/10.1007/s11104-010-0691-9
Article CAS Google Scholar

Download references

Acknowledgements

This research was supported by the Office of Science (BER), U.S. Department of Energy, grant no. DE-SC0014108. We would also like to acknowledge three anonymous reviewers for their constructive feedback which greatly improved the quality of this manuscript.

Author information

Authors and Affiliations

Department of Plant Biology, Michigan State University, 612 Wilson Rd, East Lansing, MI, 48824, USA
Alan W. Bowsher & Maren L. Friesen
Kellogg Biological Station, Hickory Corners, MI, USA
Sarah Evans
Department of Plant, Soil, and Microbial Sciences, Michigan State University, East Lansing, MI, USA
Lisa K. Tiemann
Department of Plant Pathology and Department of Crop and Soil Sciences, Washington State University, Pullman, WA, USA
Maren L. Friesen

Authors

Alan W. Bowsher
View author publications
You can also search for this author in PubMed Google Scholar
Sarah Evans
View author publications
You can also search for this author in PubMed Google Scholar
Lisa K. Tiemann
View author publications
You can also search for this author in PubMed Google Scholar
Maren L. Friesen
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alan W. Bowsher.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Eric Paterson

Electronic supplementary materials

ESM 1

(XLSX 58 kb)

ESM 2

(PDF 133 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bowsher, A.W., Evans, S., Tiemann, L.K. et al. Effects of soil nitrogen availability on rhizodeposition in plants: a review. Plant Soil 423, 59–85 (2018). https://doi.org/10.1007/s11104-017-3497-1

Download citation

Received: 18 April 2017
Accepted: 10 November 2017
Published: 20 November 2017
Issue Date: February 2018
DOI: https://doi.org/10.1007/s11104-017-3497-1

Keywords

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Effects of soil nitrogen availability on rhizodeposition in plants: a review