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Carbon flow in the rhizosphere: carbon trading at the soil–root interface

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Abstract

The loss of organic and inorganic carbon from roots into soil underpins nearly all the major changes that occur in the rhizosphere. In this review we explore the mechanistic basis of organic carbon and nitrogen flow in the rhizosphere. It is clear that C and N flow in the rhizosphere is extremely complex, being highly plant and environment dependent and varying both spatially and temporally along the root. Consequently, the amount and type of rhizodeposits (e.g. exudates, border cells, mucilage) remains highly context specific. This has severely limited our capacity to quantify and model the amount of rhizodeposition in ecosystem processes such as C sequestration and nutrient acquisition. It is now evident that C and N flow at the soil–root interface is bidirectional with C and N being lost from roots and taken up from the soil simultaneously. Here we present four alternative hypotheses to explain why high and low molecular weight organic compounds are actively cycled in the rhizosphere. These include: (1) indirect, fortuitous root exudate recapture as part of the root’s C and N distribution network, (2) direct re-uptake to enhance the plant’s C efficiency and to reduce rhizosphere microbial growth and pathogen attack, (3) direct uptake to recapture organic nutrients released from soil organic matter, and (4) for inter-root and root–microbial signal exchange. Due to severe flaws in the interpretation of commonly used isotopic labelling techniques, there is still great uncertainty surrounding the importance of these individual fluxes in the rhizosphere. Due to the importance of rhizodeposition in regulating ecosystem functioning, it is critical that future research focuses on resolving the quantitative importance of the different C and N fluxes operating in the rhizosphere and the ways in which these vary spatially and temporally.

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References

  • Abuzinadah RA, Read DJ (1989) Carbon transfer associated with assimilation of organic nitrogen sources by silver birch (Betula pendula Roth.). Trees (Berl) 3:17–23 doi:10.1007/BF00202396

    Google Scholar 

  • Ahonen-Jonnarth U, Van Hees PAW, Lundström US, Finlay RD (2000) Production of organic acids by mycorrhizal and non-mycorrhizal Pinus sylvestris L. seedlings exposed to elevated concentrations of aluminium and heavy metals. New Phytol 146:557–567 doi:10.1046/j.1469-8137.2000.00653.x

    CAS  Google Scholar 

  • Allard V, Robin C, Newton PCD, Lieffering M, Soussana JF (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 doi:10.1016/j.soilbio.2005.10.002

    CAS  Google Scholar 

  • Amiro BD, Ewing LL (1992) Physiological conditions and uptake of inorganic 14C by plant–roots. Environ Exp Bot 32:203–211 doi:10.1016/0098-8472(92)90003-K

    CAS  Google Scholar 

  • Andersson P, Berggren D (2005) Amino acids, total organic and inorganic nitrogen in forest floor soil solution at low and high nitrogen input. Water Air Soil Pollut 162:369–384 doi:10.1007/s11270-005-7372-y

    CAS  Google Scholar 

  • Antunes PM, Rajcan I, Goss MJ (2006) Specific flavonoids as interconnecting signals in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, Bradyrhizobium japonicum (Kirchner) Jordan and soybean (Glycine max (L.) Merr.). Soil Biol Biochem 38:533–543 doi:10.1016/j.soilbio.2005.06.008

    CAS  Google Scholar 

  • Bacic A, Moody SF, McComb JA, Hinch JM, Clarke AE (1987) Extracellular polysaccharides from shaken liquid cultures of Zea mays. Aust J Plant Physiol 14:633–641

    Article  CAS  Google Scholar 

  • Bahyrycz A, Konopinska D (2007) Plant signalling peptides: some recent developments. J Pept Sci 13:787–797 doi:10.1002/psc.915

    PubMed  CAS  Google Scholar 

  • Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32 doi:10.1016/j.tplants.2003.11.008

    PubMed  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 doi:10.1016/0038-0717(92)90264-X

    Google Scholar 

  • Barber SA (1995) Soil nutrient bioavailability. Wiley, New York

    Google Scholar 

  • Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84:1277–1287 doi:10.1890/0012-9658(2003)084[1277:SMCEWP]2.0.CO;2

    Google Scholar 

  • Barlow PW (1975) The root cap. In: Torrey JG, Clarkson DT (ed) The development and function of roots (Third Cabot Symposium). Academic, London, pp 21–54

    Google Scholar 

  • Beemster GTS, Baskin TI (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol 116:1515–1526 doi:10.1104/pp.116.4.1515

    PubMed  CAS  Google Scholar 

  • Bending GD, Read DJ (1995) The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. The foraging behaviour of ectomycorrhizal mycelium and the translocation of nutrients from exploited organic matter. New Phytol 130:401–409 doi:10.1111/j.1469-8137.1995.tb01834.x

    CAS  Google Scholar 

  • Bengough AG, Kirby JM (1999) Tribology of the root cap in maize (Zea mays) and peas (Pisum sativum). New Phytol 142:421–425 doi:10.1046/j.1469-8137.1999.00406.x

    Google Scholar 

  • Bengough AG, McKenzie BM (1997) Sloughing of root cap cells decreases the frictional resistance to maize (Zea mays L.) root growth. J Exp Bot 48:885–893 doi:10.1093/jxb/48.4.885

    CAS  Google Scholar 

  • Bidartondo MI (2005) The evolutionary ecology of mycoheterotrophy. New Phytol 167:335–352 doi:10.1111/j.1469-8137.2005.01429.x

    PubMed  Google Scholar 

  • Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Domínguez L, Sérsic A, Leake JR, Read DJ (2002) Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:389–392 doi:10.1038/nature01054

    PubMed  CAS  Google Scholar 

  • Bidel LPR, Pages L, Riviere LM, Pelloux G, Lorendeau JY (2000) MassFlowDyn I: A carbon transport and partitioning model for root system architecture. Ann Bot (Lond) 85:869–886 doi:10.1006/anbo.2000.1149

    CAS  Google Scholar 

  • Bockenhoff A, Prior DAM, Grundler FMW, Oparka KJ (1996) Induction of phloem unloading in Arabidopsis thaliana roots by the parasitic nematode Heterodera schachtii. Plant Physiol 112:1421–1427 doi:10.1104/pp.112.4.1421

    PubMed  CAS  Google Scholar 

  • Boddy E, Hill PW, Farrar J, Jones DL (2007) Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field soils. Soil Biol Biochem 39:827–835 doi:10.1016/j.soilbio.2006.09.030

    CAS  Google Scholar 

  • Boutton TW (1996) Stable carbon isotope ratios of soil organic matter and their use as indicators of vegetation and climate change. In: Boutton TW, Yamasaki S (eds) Mass spectrometry of soils. Marcel Dekker, New York, pp 47–82

    Google Scholar 

  • Bouwmeester HJ, Roux C, Lopez-Raez JA, Bécard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230 doi:10.1016/j.tplants.2007.03.009

    PubMed  CAS  Google Scholar 

  • Brigham LA, Woo H, Nicoll SM, Hawes MC (1995) Differential expression of proteins and mRNAs from border cells and root tips of pea. Plant Physiol 109:457–463

    PubMed  CAS  Google Scholar 

  • Brown ME (1972) Plant-growth substances produced by microorganisms of soil and rhizosphere. J Appl Bacteriol 35:443–451

    CAS  Google Scholar 

  • Buer CS, Muday GK, Djordjevic MA (2007) Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiol 145:478–490 doi:10.1104/pp.107.101824

    PubMed  CAS  Google Scholar 

  • Canny MJ (1995) Apoplastic water and solute movement—new rules for an old space. Annu Rev Plant Physiol Plant Mol Biol 46:215–236 doi:10.1146/annurev.pp.46.060195.001243

    CAS  Google Scholar 

  • Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a nonmycorrhizal arctic sedge. Nature 361:150–153 doi:10.1038/361150a0

    CAS  Google Scholar 

  • Cheng WX, Coleman DC, Carroll CR, Hoffman C (1993) In-situ measurement of root respiration and soluble C-concentrations in the rhizosphere. Soil Biol Biochem 25:1189–1196 doi:10.1016/0038-0717(93)90251-6

    Google Scholar 

  • Ciereszko I, Farrar JF, Rychter AM (1999) Compartmentation and fluxes of sugars in roots of Phaseolus vulgaris under phosphate deficiency. Biol Plant 42:223–231 doi:10.1023/A:1002108601862

    CAS  Google Scholar 

  • Clark FE (1949) Soil microorganisms and plant roots. Adv Agron 1:241–288 doi:10.1016/S0065-2113(08)60750-6

    CAS  Google Scholar 

  • Cram WJ (1974) Effects of Cl on HCO3 and malate fluxes and CO2 fixation in carrot and barley root cells. J Exp Bot 25:253–268 doi:10.1093/jxb/25.2.253

    CAS  Google Scholar 

  • Curl EA, Truelove (1986) The rhizosphere. Advanced series in agricultural science 15. Springer, Berlin

    Google Scholar 

  • 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

    Google Scholar 

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47 doi:10.1023/A:1020809400075

    CAS  Google Scholar 

  • Darrah PR (1991a) Models of the rhizosphere. 1. Microbial-population dynamics around a root releasing soluble and insoluble carbon. Plant Soil 133:187–199 doi:10.1007/BF00009191

    CAS  Google Scholar 

  • Darrah PR (1991b) Models of the rhizosphere. 2. A quasi 3-dimensional simulation of the microbial-population dynamics around a growing root releasing soluble exudates. Plant Soil 138:147–158 doi:10.1007/BF00012241

    Google Scholar 

  • Darrah PR, Jones DL, Kirk GJD, Roose T (2006) Modelling the rhizosphere: a review of methods for ‘upscaling’ to the whole-plant scale. Eur J Soil Sci 57:13–25 doi:10.1111/j.1365-2389.2006.00786.x

    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 doi:10.1093/jxb/54.381.325

    PubMed  CAS  Google Scholar 

  • de Graaff MA, Six J, van Kessel C (2007) Elevated CO2 increases nitrogen rhizodeposition and microbial immobilization of root-derived nitrogen. New Phytol 173:778–786 doi:10.1111/j.1469-8137.2006.01974.x

    PubMed  Google Scholar 

  • Derrien D, Marol C, Balesdent J (2004) The dynamics of neutral sugars in the rhizosphere of wheat. An approach by 13C pulse-labelling and GC/C/IRMS. Plant Soil 267:243–253 doi:10.1007/s11104-005-5348-8

    CAS  Google Scholar 

  • Dilkes NB, Jones DL, Farrar J (2004) Temporal dynamics of carbon partitioning and rhizodeposition in wheat. Plant Physiol 134:706–715 doi:10.1104/pp.103.032045

    PubMed  CAS  Google Scholar 

  • Dilworth MJ, James EK, Sprent JI, Newton WE (2008) Nitrogen-fixing leguminous symbioses. Springer, New York

    Google Scholar 

  • Dimou M, Flemetakis E, Delis C, Aivalakis G, Spyropoulos KG, Katinakis P (2005) Genes coding for a putative cell-wall invertase and two putative monosaccharide/H+ transporters are expressed in roots of etiolated Glycine max seedlings. Plant Sci 169:798–804 doi:10.1016/j.plantsci.2005.05.037

    CAS  Google Scholar 

  • DiTomaso JM, Hart JJ, Kochian LV (1992) Transport kinetics and metabolism of exogenously applied putrescine in roots of intact maize seedlings. Plant Physiol 98:611–620 doi:10.1104/pp.98.2.611

    PubMed  CAS  Google Scholar 

  • Ekblad A, Hogberg P (2001) Natural abundance of 13C in CO2 respired from forest soils reveals speed of link between tree photosynthesis and root respiration. Oecologia 127:305–308 doi:10.1007/s004420100667

    Google Scholar 

  • Eleftheriou EP, Lazarou DS (1997) Cytochemical localization of ATPase activity in roots of wheat (Triticum aestivum). Biologia 52:573–583

    CAS  Google Scholar 

  • Emerson D, Agulto L, Liu H, Liu LP (2008) Identifying and characterizing bacteria in an era of genomics and proteomics. Bioscience 58:925–936 doi:10.1641/B581006

    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 doi:10.1890/0012-9658(2003)084[0827:HRCTFO]2.0.CO;2

    Google Scholar 

  • Faure D, Bloemberg G, Leveau J, Veereecke D (2009) Molecular communications in the rhizosphere. Plant Soil (this volume)

  • Feng JN, Volk RJ, Jackson WA (1994) Inward and outward transport of ammonium in roots of maize and sorghum—contrasting effects of methionine sulfoximine. J Exp Bot 45:429–439 doi:10.1093/jxb/45.4.429

    CAS  Google Scholar 

  • Filion M, St-Arnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere micro-organisms. New Phytol 141:525–533 doi:10.1046/j.1469-8137.1999.00366.x

    Google Scholar 

  • Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126 doi:10.1093/jxb/ern059

    PubMed  CAS  Google Scholar 

  • Finlay RD, Rosling A (2006) Integrated nutrient cycles in forest ecosystems, the role of ectomycorrhizal fungi. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, Cambridge, pp 28–50

    Google Scholar 

  • Finlay R, Söderström B (1992) Mycorrhiza and carbon flow to the soil. In: Allen MJ (ed) Mycorrhizal functioning. Chapman & Hall, New York, pp 134–160

    Google Scholar 

  • Fischer WN, Andre B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K, Frommer WB (1998) Amino acid transport in plants. Trends Plant Sci 3:188–195 doi:10.1016/S1360-1385(98)01231-X

    Google Scholar 

  • Fleischer A, Ehwald R (1995) The free-space of sugars in plant-tissues—external film and apoplastic volume. J Exp Bot 46:647–654 doi:10.1093/jxb/46.6.647

    CAS  Google Scholar 

  • Ford CR, Wurzburger N, Hendrick RL, Teskey RO (2007) Soil DIC uptake and fixation in Pinus taeda seedlings and its C contribution to plant tissues and ectomycorrhizal fungi. Tree Physiol 27:375–383

    PubMed  CAS  Google Scholar 

  • Francis R, Read DJ (1984) Direct transfer of carbon between plants connected by vesicular arbuscular mycorrhizal mycelium. Nature 307:53–56 doi:10.1038/307053a0

    CAS  Google Scholar 

  • Fulthorpe RR, Roesch LFW, Riva A, Triplett EW (2008) Distantly sampled soils carry few species in common. ISME J 2:901–910 doi:10.1038/ismej.2008.55

    PubMed  CAS  Google Scholar 

  • Fusseder A (1987) The longevity and activity of the primary root of maize. Plant Soil 101:257–265 doi:10.1007/BF02370653

    Google Scholar 

  • Gaudinski JB, Trumbore SE, Davidson EA, Cook AC, Markewitz D, Richter DD (2001) The age of fine-root carbon in three forests of the eastern United States measured by radiocarbon. Oecologia 129:420–429

    Google Scholar 

  • Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147:13–31 doi:10.1046/j.1469-8137.2000.00681.x

    Google Scholar 

  • Godbold DL, Hoosbeek MR, Lukac M, Cotrufo MF, Janssens IA, Ceulemans R, Polle A, Velthorst EJ, Scarascia-Mugnozza G, DeAngelis P, Miglietta F, Peressotti A (2006) Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 281:15–24 doi:10.1007/s11104-005-3701-6

    CAS  Google Scholar 

  • Gout E, Bligny R, Pascal N, Douce R (1993) 13C nuclear-magnetic-resonance studies of malate and citrate synthesis and compartmentation in higher-plant cells. J Biol Chem 268:3986–3992

    PubMed  CAS  Google Scholar 

  • Grant RF (1993) Rhizodeposition by crop plants and its relationship to microbial activity and nitrogen distribution. Model Geo-Biosph Process 2:193–209

    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 doi:10.1016/S0929-1393(96)00126-6

    Google Scholar 

  • Guckert A, Breisch H, Reisinger O (1975) Soil/root interface. 1. Electron microscope study of mucigel/clay micro-organism relations. Soil Biol Biochem 7:241–250 doi:10.1016/0038-0717(75)90061-9

    Google Scholar 

  • Gunawardena U, Hawes MC (2002) Tissue specific localization of root infection by fungal pathogens: role of root border cells. Mol Plant Microbe Interact 15:1128–1136 doi:10.1094/MPMI.2002.15.11.1128

    PubMed  CAS  Google Scholar 

  • Hart JJ, DiTomaso JM, Linscott DL, Kochian LV (1992) Transport interactions between paraquat and polyamines in roots of intact maize seedlings. Plant Physiol 99:1400–1405 doi:10.1104/pp.99.4.1400

    PubMed  CAS  Google Scholar 

  • Hartmann A, Berg G, van Tuinen D (2009) Plant-driven selection of microbes. Plant Soil (this volume)

  • Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Z (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Annu Rev Phytopathol 36:311–327 doi:10.1146/annurev.phyto.36.1.311

    PubMed  CAS  Google Scholar 

  • Hawes MC, Gunawardena U, Miyasaka S, Zhao XW (2000) The role of root border cells in plant defence. Trends Plant Sci 5:128–133 doi:10.1016/S1360-1385(00)01556-9

    PubMed  CAS  Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506 doi:10.1111/j.1469-8137.2007.02051.x

    PubMed  CAS  Google Scholar 

  • Henry F, Nguyen C, Paterson E, Sim A, Robin C (2005) How does nitrogen availability alter rhizodeposition in Lolium multiflorum Lam. during vegetative growth? Plant Soil 269:181–191 doi:10.1007/s11104-004-0490-2

    CAS  Google Scholar 

  • Herrmann A, Felle HH (1995) Tip growth in root hair-cells of Sinapis-alba. l—significance of internal and external Ca2+ and pH. New Phytol 129:523–533 doi:10.1111/j.1469-8137.1995.tb04323.x

    CAS  Google Scholar 

  • Hertenberger G, Wanek W (2004) Evaluation of methods to measure differential 15N labeling of soil and root N pools for studies of root exudation. Rapid Commun Mass Spectrom 18:2415–2425 doi:10.1002/rcm.1615

    PubMed  CAS  Google Scholar 

  • Hill PW, Marshall C, Williams GG, Blum H, Harmens H, Jones DL, Farrar JF (2007) The fate of photosynthetically-fixed carbon in Lolium perenne grassland as modified by elevated CO2 and sward management. New Phytol 173:766–777 doi:10.1111/j.1469-8137.2007.01966.x

    PubMed  CAS  Google Scholar 

  • Hill PW, Farrar JF, Jones DL (2008) Decoupling of microbial glucose uptake and mineralization in soil. Soil Biol Biochem 40:616–624 doi:10.1016/j.soilbio.2007.09.008

    CAS  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195 doi:10.1023/A:1013351617532

    CAS  Google Scholar 

  • Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil (this volume)

  • Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946 doi:10.1105/tpc.106.041012

    PubMed  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 doi:10.1007/BF00029278

    CAS  Google Scholar 

  • Hodge A, Paterson E, Thornton B, Millard P, Killham K (1997) Effects of photon flux density on carbon partitioning and rhizosphere carbon flow of Lolium perenne. J Exp Bot 48:1797–1805

    CAS  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299 doi:10.1038/35095041

    PubMed  CAS  Google Scholar 

  • Hoffland E, Findenegg GR, Nelemans JA (1989) Solubilization of rock phosphate by rape. 2. Local root exudation of organic-acids as a response to P-starvation. Plant Soil 113:161–165 doi:10.1007/BF02280176

    CAS  Google Scholar 

  • Högberg MN, Högberg P (2002) Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol 154:791–795 doi:10.1046/j.1469-8137.2002.00417.x

    Google Scholar 

  • Högberg P, Read DJ (2006) Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–554 doi:10.1016/j.tree.2006.06.004

    PubMed  Google Scholar 

  • Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792 doi:10.1038/35081058

    PubMed  Google Scholar 

  • Högberg P, Högberg MN, Göttlicher SG, Betson NR, Keel SG, Metcalfe DB, Campbell C, Schindlbacher A, Hurry V, Lundmark T, Linder S, Näsholm T (2008) High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytol 177:220–228

    PubMed  Google Scholar 

  • Hogh-Jensen H, Schjoerring JK (2001) Rhizodeposition of nitrogen by red clover, white clover and ryegrass leys. Soil Biol Biochem 33:439–448 doi:10.1016/S0038-0717(00)00183-8

    CAS  Google Scholar 

  • Huang LF, Bocock PN, Davis JM, Koch KE (2007) Regulation of invertase: a suite of transcriptional and post-transcriptional mechanisms. Funct Plant Biol 34:499–507 doi:10.1071/FP06227

    CAS  Google Scholar 

  • Hukin D, Doering-Saad C, Thomas CR, Pritchard J (2002) Sensitivity of cell hydraulic conductivity to mercury is coincident with symplasmic isolation and expression of plasmalemma aquaporin genes in growing maize roots. Planta 215:1047–1056 doi:10.1007/s00425-002-0841-2

    PubMed  CAS  Google Scholar 

  • Iijima M, Griffiths B, Bengough AG (2000) Sloughing of cap cells and carbon exudation from maize seedling roots in compacted sand. New Phytol 145:477–482 doi:10.1046/j.1469-8137.2000.00595.x

    Google Scholar 

  • Iijima M, Higuchi T, Barlow PW (2004) Contribution of root cap mucilage and presence of an intact root cap in maize (Zea mays) to the reduction of soil mechanical impedance. Ann Bot (Lond) 94:473–477 doi:10.1093/aob/mch166

    Google Scholar 

  • Jahn T, Baluska F, Michalke W, Harper JF, Volkmann D (1998) Plasma membrane H+-ATPase in the root apex: evidence for strong expression in xylem parenchyma and asymmetric localization within cortical and epidermal cells. Physiol Plant 104:311–316 doi:10.1034/j.1399-3054.1998.1040304.x

    CAS  Google Scholar 

  • Jensen ES (1996) Rhizodeposition of N by pea and barley and its effect on soil N dynamics. Soil Biol Biochem 28:65–71 doi:10.1016/0038-0717(95)00116-6

    CAS  Google Scholar 

  • Jiang K, Zhang SB, Lee S, Tsai G, Kim K, Huang HY, Chilcott C, Zhu T, Feldman LJ (2006) Transcription profile analyses identify genes and pathways central to root cap functions in maize. Plant Mol Biol 60:343–363 doi:10.1007/s11103-005-4209-4

    PubMed  CAS  Google Scholar 

  • Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13 doi:10.1016/j.femsec.2003.11.012

    CAS  PubMed  Google Scholar 

  • Johnson JF, Allan DL, Vance CP, Weiblen G (1996) Root carbon dioxide fixation by phosphorus-deficient Lupinus albus—contribution to organic acid exudation by proteoid roots. Plant Physiol 112:19–30 doi:10.1104/pp.112.1.31

    PubMed  CAS  Google Scholar 

  • Johnson D, Leake JR, Ostle N, Ineson P, Read DJ (2002) In situ 13CO2 pulse-labelling of upland grassland demonstrates that a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327–334 doi:10.1046/j.0028-646X.2001.00316.x

    CAS  Google Scholar 

  • Johnson D, Krsek M, Wellington EMH, Stott AW, Cole L, Bardgett RD, Read DJ, Leake JR (2005) Soil invertebrates disrupt carbon flow through fungal networks. Science 309:1047 doi:10.1126/science.1114769

    PubMed  CAS  Google Scholar 

  • Jones DL, Darrah PR (1992) Resorption of organic-components by roots of Zea mays L. and its consequences in the rhizosphere. 1. Resorption of 14C labelled glucose, mannose and citric-acid. Plant Soil 143:259–266 doi:10.1007/BF00007881

    CAS  Google Scholar 

  • Jones DL, Darrah PR (1993) Re-sorption of organic-compounds by roots of Zea mays L. and its consequences in the rhizosphere. 2. Experimental and model evidence for simultaneous exudation and re-sorption of soluble C compounds. Plant Soil 153:47–59 doi:10.1007/BF00010543

    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

    CAS  Google Scholar 

  • Jones DL, Darrah PR (1995) Influx and efflux of organic-acids across the soil–root interface of Zea mays L. and its implications in rhizosphere C flow. Plant Soil 173:103–109 doi:10.1007/BF00155523

    CAS  Google Scholar 

  • Jones DL, Darrah PR (1996) Re-sorption of organic compounds by roots of Zea mays L. and its consequences in the rhizosphere. 3. Characteristics of sugar influx and efflux. Plant Soil 178:153–160 doi:10.1007/BF00011173

    CAS  Google Scholar 

  • Jones DL, Darrah PR, Kochian LV (1996) Critical evaluation of organic acid mediated iron dissolution in the rhizosphere and its potential role in root iron uptake. Plant Soil 180:57–66

    CAS  Google Scholar 

  • 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  Google Scholar 

  • Jones DL, Healey JR, Willett VB, Farrar JF (2005a) Dissolved organic nitrogen uptake by plants—an important N uptake pathway? Soil Biol Biochem 37:413–423 doi:10.1016/j.soilbio.2004.08.008

    CAS  Google Scholar 

  • Jones DL, Shannon D, Junvee-Fortune T, Farrar JF (2005b) Plant capture of free amino acids is maximized under high soil amino acid concentrations. Soil Biol Biochem 37:179–181 doi:10.1016/j.soilbio.2004.07.021

    CAS  Google Scholar 

  • Jun JH, Fiume E, Fletcher JC (2008) The CLE family of plant polypeptide signalling molecules. Cell Mol Life Sci 65:743–755 doi:10.1007/s00018-007-7411-5

    PubMed  CAS  Google Scholar 

  • Knox OGG, Gupta VVSR, Nehl DB, Stiller WN (2007) Constitutive expression of Cry proteins in roots and border cells of transgenic cotton. Euphytica 154:83–90 doi:10.1007/s10681-006-9272-7

    CAS  Google Scholar 

  • Körner C, Asshoff R, Bignucolo O, Hättenschwiler R, Keel SG, Peláez-Riedl S, Pepin S, Siegwolf RTW, Zotz G (2005) Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2. Science 309:1360–1362

    PubMed  Google Scholar 

  • Kraffczyk I, Trolldenier G, Beringer H (1984) Soluble root exudates of maize: influence of potassium supply and rhizosphere microorganisms. Soil Biol Biochem 16:315–322 doi:10.1016/0038-0717(84)90025-7

    CAS  Google Scholar 

  • Kramer EM, Frazer NL, Baskin TI (2007) Measurement of diffusion within the cell wall in living roots of Arabidopsis thaliana. J Exp Bot 58:3005–3015 doi:10.1093/jxb/erm155

    PubMed  CAS  Google Scholar 

  • Kuzyakov Y (2002) Separating microbial respiration of exudates from root respiration in non-sterile soils: a comparison of four methods. Soil Biol Biochem 34:1621–1631 doi:10.1016/S0038-0717(02)00146-3

    CAS  Google Scholar 

  • Kuzyakov Y (2006) Sources of CO2 efflux from soil and review of partitioning methods. Soil Biol Biochem 38:425–448 doi:10.1016/j.soilbio.2005.08.020

    CAS  Google Scholar 

  • 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  Google Scholar 

  • Kuzyakov Y, Jones DL (2006) Glucose uptake by maize roots and its transformation in the rhizosphere. Soil Biol Biochem 38:851–860 doi:10.1016/j.soilbio.2005.07.012

    CAS  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103 doi:10.1016/j.tree.2007.10.008

    PubMed  Google Scholar 

  • Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant–microbe–soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil (this volume)

  • Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Environ Qual 31:109–120

    Article  PubMed  CAS  Google Scholar 

  • Leake JR (2004) Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi. Curr Opin Plant Biol 7:422–428 doi:10.1016/j.pbi.2004.04.004

    PubMed  CAS  Google Scholar 

  • Leake JR, Donnelly DP, Saunders EM, Boddy L, Read DJ (2001) Rates and quantities of carbon flux to ectomycorrhizal mycelium following 14C pulse labeling of Pinus sylvestris seedlings: effects of litter patches and interaction with a wood decomposer fungus. Tree Physiol 21:71–82

    PubMed  CAS  Google Scholar 

  • Leake JR, Johnson D, Donnelly D, Muckle G, Boddy L, Read DJ (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82:1016–1045 doi:10.1139/b04-060

    Google Scholar 

  • Leinweber P, Eckhardt KU, Fischer H, Kuzyakov Y (2008) A new rapid micro-method for the molecular–chemical characterization of rhizodeposits by field-ionization mass spectrometry. Rapid Commun Mass Spectrom 22:1230–1234 doi:10.1002/rcm.3463

    PubMed  CAS  Google Scholar 

  • Ligaba A, Katsuhara M, Ryan PR, Shibasaka M, Matsumoto H (2006) The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells. Plant Physiol 142:1294–1303 doi:10.1104/pp.106.085233

    PubMed  CAS  Google Scholar 

  • Lindahl B, Olsson S, Stenlid J, Finlay RD (2001) Effects of resource availability on mycelial interactions and 32P-transfer between a saprotrophic and an ectomycorrhizal fungus in soil microcosms. FEMS Microbiol Ecol 38:43–52 doi:10.1111/j.1574-6941.2001.tb00880.x

    CAS  Google Scholar 

  • Lindahl BD, Finlay RD, Cairney JWG (2005) Enzymatic activities of mycelia in mycorrhizal fungal communities. In: Dighton J, Oudemans P, White J (eds) The fungal community: its organization and role in the ecosystem. Marcel Dekker, New York, pp 331–348

    Google Scholar 

  • Lindahl BD, Ihrmark K, Boberg J, Trumbore S, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in boreal forests. New Phytol 173:611–620 doi:10.1111/j.1469-8137.2006.01936.x

    PubMed  CAS  Google Scholar 

  • Lipson D, Nasholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128:305–316 doi:10.1007/s004420100693

    Google Scholar 

  • Lynch JM (1990) The rhizosphere. Wiley, London

    Google Scholar 

  • Martin JK (1975) 14C-labeled material leached from rhizosphere of plants supplied continuously with 14CO2. Soil Biol Biochem 7:395–399 doi:10.1016/0038-0717(75)90056-5

    CAS  Google Scholar 

  • Mary B, Mariotti A, Morel JL (1992) Use of 13C variations at natural abundance for studying the biodegradation of root mucilage, roots and glucose in soil. Soil Biol Biochem 24:1065–1072 doi:10.1016/0038-0717(92)90037-X

    Google Scholar 

  • Mary B, Fresneau C, Morel JL, Mariotti A (1993) C-cycling and N-cycling during decomposition of root mucilage, roots and glucose in soil. Soil Biol Biochem 25:1005–1014 doi:10.1016/0038-0717(93)90147-4

    CAS  Google Scholar 

  • Matiru VN, Dakora FD (2005) The rhizosphere signal molecule lumichrome alters seedling development in both legumes and cereals. New Phytol 166:439–444 doi:10.1111/j.1469-8137.2005.01344.x

    PubMed  CAS  Google Scholar 

  • Mayer J, Buegger F, Jensen ES, Schloter M, Hess J (2003) Estimating N rhizodeposition of grain legumes using a 15N in situ stem labelling method. Soil Biol Biochem 35:21–28 doi:10.1016/S0038-0717(02)00212-2

    CAS  Google Scholar 

  • McClaugherty CA, Aber JD, Melillo JM (1982) The role of fine roots in the organic-matter and nitrogen budgets of 2 forested ecosystems. Ecology 63:1481–1490 doi:10.2307/1938874

    Google Scholar 

  • McCully ME (1999) Roots in soil: unearthing the complexities of roots and their rhizospheres. Annu Rev Plant Physiol Plant Mol Biol 50:695–718 doi:10.1146/annurev.arplant.50.1.695

    PubMed  CAS  Google Scholar 

  • McCully ME, Boyer JS (1997) The expansion of maize root-cap mucilage during hydration. 3. Changes in water potential and water content. Physiol Plant 99:169–177 doi:10.1111/j.1399-3054.1997.tb03445.x

    CAS  Google Scholar 

  • McCully ME, Canny MJ (1985) Localisation of translocated 14C in roots and root exudates of field-grown maize. Physiol Plant 65:380–392 doi:10.1111/j.1399-3054.1985.tb08661.x

    CAS  Google Scholar 

  • McDougal BM, Rovira AD (1970) Sites of exudation of 14C-labelled compounds from wheat roots. New Phytol 69:999–1002 doi:10.1111/j.1469-8137.1970.tb02479.x

    Google Scholar 

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

    CAS  Google Scholar 

  • Meldrum D (2000) Automation for genomics, part two: sequencers, microarrays, and future trends. Genome Res 10:1288–1303 doi:10.1101/gr.157400

    PubMed  CAS  Google Scholar 

  • Mench M, Morel JL, Guckert A (1987) Metal binding properties of high molecular weight soluble exudates from maize (Zea mays L.) roots. Biol Fertil Soils 3:165–169 doi:10.1007/BF00255778

    CAS  Google Scholar 

  • Miyasaka SC, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125:1978–1987 doi:10.1104/pp.125.4.1978

    PubMed  CAS  Google Scholar 

  • Morel JL, Mench M, Guckert A (1986) Measurement of Pb2+, Cu2+ and Cd2+ binding with mucilage exudates from maize (Zea mays L.) roots. Biol Fertil Soils 2:29–34 doi:10.1007/BF00638958

    Google Scholar 

  • Morel HJL, Guckert A, Plantureux S, Chenu C (1990) Influence of root exudates on soil aggregation. Symbiosis 9:87–91

    Google Scholar 

  • Morre DJ, Jones DD, Mollenhauer HH (1967) Golgi apparatus mediated polysaccharide secretion by outer root cap cells of Zea mays. 1. Kinetics and secretory pathway. Planta 74:286–301 doi:10.1007/BF00384849

    CAS  Google Scholar 

  • Nadelhoffer KJ, Raich JW (1992) Fine root production estimates and belowground carbon allocation in forest ecosystems. Ecology 73:1139–1147 doi:10.2307/1940664

    Google Scholar 

  • Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392:914–916 doi:10.1038/31921

    Google Scholar 

  • Negishi T, Nakanishi H, Yazaki J, Kishimoto N, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kikuchi S, Mori S, Nishizawa NK (2002) cDNA microarray analysis of gene expression during Fe-deficiency stress in barley suggests that polar transport of vesicles is implicated in phytosiderophore secretion in Fe-deficient barley roots. Plant J 30:83–94 doi:10.1046/j.1365-313X.2002.01270.x

    PubMed  CAS  Google Scholar 

  • Nehls U (2008) Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. J Exp Bot 59:1097–1108 doi:10.1093/jxb/erm334

    PubMed  CAS  Google Scholar 

  • Neumann G, Römheld V (2001) The release of root exudates as affected by the plant’s physiological status. In: Pinton R, Varini Z, Nannipieri P (eds) The rhizosphere. Biochemistry and organic substances at the soil–plant interface. Marcel Dekker, New York, pp 41–93

    Google Scholar 

  • Newman EI, Watson A (1977) Microbial abundance in rhizosphere—computer-model. Plant Soil 48:17–56 doi:10.1007/BF00015157

    Google Scholar 

  • Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396 doi:10.1051/agro:2003011

    CAS  Google Scholar 

  • Nguyen C, Guckert A (2001) Short-term utilisation of C-14-[U]glucose by soil microorganisms in relation to carbon availability. Soil Biol Biochem 33:53–60 doi:10.1016/S0038-0717(00)00114-0

    CAS  Google Scholar 

  • Nguyen C, Froux F, Recous S, Morvan T, Robin C (2008) Net N immobilisation during the biodegradation of mucilage in soil as affected by repeated mineral and organic fertilization. Nutr Cycl Agroecosyst 80:39–47 doi:10.1007/s10705-007-9119-1

    Google Scholar 

  • Nye PH, Tinker PB (2000) Solute movement in the rhizosphere. Oxford University Press, Oxford

    Google Scholar 

  • Offre P, Pivato B, Mazurier S, Siblot S, Berta G, Lemanceau P, Mougel C (2008) Microdiversity of Burkholderiales associated with mycorrhizal and nonmycorrhizal roots of Medicago truncatula. FEMS Microbiol Ecol 65:180–192 doi:10.1111/j.1574-6941.2008.00504.x

    PubMed  CAS  Google Scholar 

  • Ohyama T, Ohtake T, Sueyoshi K, Tewari K, Takahashi Y, Ito S, Nishiwaki T, Nagumo Y, Ishii S, Sato T (2009) Nitrogen fixation and metabolism in soybean plants. Nova, Hauppauge

    Google Scholar 

  • Oksman-Caldentey KM, Inze D (2004) Plant cell factories in the post-genomic era: new ways to produce designer secondary metabolites. Trends Plant Sci 9:433–440 doi:10.1016/j.tplants.2004.07.006

    PubMed  CAS  Google Scholar 

  • Ostle N, Whiteley AS, Bailey MJ, Sleep D, Ineson P, Manefield M (2003) Active microbial RNA turnover in a grassland soil estimated using a 13CO2 spike. Soil Biol Biochem 35:877–885 doi:10.1016/S0038-0717(03)00117-2

    CAS  Google Scholar 

  • Ovecka M, Lang I, Baluska F, Ismail A, Illes P, Lichtscheidl IK (2005) Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 226:39–54 doi:10.1007/s00709-005-0103-9

    PubMed  CAS  Google Scholar 

  • Owen AG, Jones DL (2001) Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biol Biochem 33:651–657 doi:10.1016/S0038-0717(00)00209-1

    CAS  Google Scholar 

  • Pages L, Pellerin S (1996) Study of differences between vertical root maps observed in a maize crop and simulated maps obtained using a model for the three-dimensional architecture of the root system. Plant Soil 182:329–337

    CAS  Google Scholar 

  • Patel DD, Barlow PW, Lee RB (1990) Development of vacuolar volume in the root-tips of pea. Ann Bot (Lond) 65:159–169

    Google Scholar 

  • 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

    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 doi:10.1023/A:1004789407065

    CAS  Google Scholar 

  • Paterson E, Thornton B, Sim A, Pratt S (2003) Effects of defoliation and atmospheric CO2 depletion on nitrate acquisition, and exudation of organic compounds by roots of Festuca rubra. Plant Soil 250:293–305 doi:10.1023/A:1022819219947

    CAS  Google Scholar 

  • Paterson E, Thornton B, Midwood AJ, Sim A (2005) Defoliation alters the relative contributions of recent and non-recent assimilate to root exudation from Festuca rubra. Plant Cell Environ 28:1525–1533 doi:10.1111/j.1365-3040.2005.01389.x

    Google Scholar 

  • Paterson E, Sim A, Standing D, Dorward M, McDonald AJS (2006) Root exudation from Hordeum vulgare in response to localized nitrate supply. J Exp Bot 57:2413–2420 doi:10.1093/jxb/erj214

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Paterson E, Osler G, Dawson LA, Gebbing T, Sim A, Ord B (2008) Labile and recalcitrant plant fractions are utilised by distinct microbial communities in soil: independent of the presence of roots and mycorrhizal fungi. Soil Biol Biochem 40:1103–1113 doi:10.1016/j.soilbio.2007.12.003

    CAS  Google Scholar 

  • Patrick JW (1997) Phloem unloading: sieve element unloading and post-sieve element transport Ann Rev Plant Physiol. Plant Mol Biol 48:191–222 doi:10.1146/annurev.arplant.48.1.191

    CAS  Google Scholar 

  • Paull RE, Jones RL (1975a) Studies on the secretion of maize root cap slime. 2. Localization of slime production. Plant Physiol 56:307–312 doi:10.1104/pp.56.2.307

    PubMed  CAS  Google Scholar 

  • Paull RE, Jones RL (1975b) Studies on the secretion of maize root-cap slime. 3. Histochemical and autoradiographic localization of incorporated fucose. Planta 127:97–110 doi:10.1007/BF00388371

    Google Scholar 

  • Paull RE, Jones RL (1976a) Studies on the secretion of maize root cap slime. 4. Evidence for the involvement of dictyosomes. Plant Physiol 57:249–256 doi:10.1104/pp.57.2.249

    PubMed  CAS  Google Scholar 

  • Paull RE, Jones RL (1976b) Studies on the secretion of maize root cap slime. 5. The cell wall as a barrier to secretion. Zeit Pflanzenphysiol 79:154–164

    CAS  Google Scholar 

  • Paull RE, Johnson CM, Jones RL (1975) Studies on the secretion of maize root cap slime. 1. Some properties of the secreted polymer. Plant Physiol 56:300–306 doi:10.1104/pp.56.2.300

    PubMed  CAS  Google Scholar 

  • Personeni E, Nguyen C, Marchal P, Pagès L (2007) Experimental evaluation of an efflux–influx model of C exudation by individual apical root segments. J Exp Bot 58:2091–2099 doi:10.1093/jxb/erm065

    PubMed  CAS  Google Scholar 

  • Pfeffer PE, Douds DD, Bücking H, Schwartz DP, Shachar-Hill Y (2004) The fungus does not transfer carbon to or between roots in an arbuscular mycorrhizal symbiosis. New Phytol 163:617–627

    Google Scholar 

  • Philips DA, Fox TC, Six J (2006) Root exudation (net efflux of amino acids) may increase rhizodeposition under elevated CO2. Glob Change Biol 12:561–567 doi:10.1111/j.1365-2486.2006.01100.x

    Google Scholar 

  • Phillips RP, Fahey TJ (2005) Patterns of rhizosphere carbon flux in sugar maple (Acer saccharum) and yellow birch (Betula allegheniensis) saplings. Glob Change Biol 11:983–995 doi:10.1111/j.1365-2486.2005.00959.x

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Pinton R, Varanini Z, Nannipieri P (2001) The rhizosphere. Biochemistry and organic substances at the soil–plant interface. CRC, Boca Raton

    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 doi:10.1016/S0038-0717(97)00043-6

    CAS  Google Scholar 

  • Quadt-Hallmann A, Hallmann J, Kloepper JW (1997) Bacterial endophytes in cotton: location and interaction with other plant associated bacteria. Can J Microbiol 43:254–259

    Article  CAS  Google Scholar 

  • Rangel-Castro JI, Killham K, Ostle N, Nicol GW, Anderson IC, Scrimgeour CM, Ineson P, Meharg A, Prosser JI (2005a) Stable isotope probing analysis of the influence of liming on root exudate utilization by soil microorganisms. Environ Microbiol 7:828–838 doi:10.1111/j.1462-2920.2005.00756.x

    PubMed  CAS  Google Scholar 

  • Rangel-Castro JI, Prosser JI, Ostle N, Scrimgeour CM, Killham K, Meharg A (2005b) Flux and turnover of fixed carbon in soil microbial biomass of limed and unlimed plots of an upland grassland ecosystem. Environ Microbiol 7:544–552 doi:10.1111/j.1462-2920.2005.00722.x

    PubMed  CAS  Google Scholar 

  • Read DB, Gregory PJ (1997) Surface tension and viscosity of axenic maize and lupin root mucilages. New Phytol 137:623–628 doi:10.1046/j.1469-8137.1997.00859.x

    Google Scholar 

  • Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492 doi:10.1046/j.1469-8137.2003.00704.x

    Google Scholar 

  • 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  Google Scholar 

  • Roberts SK (2006) Plasma membrane anion channels in higher plants and their putative functions in roots. New Phytol 169:647–666 doi:10.1111/j.1469-8137.2006.01639.x

    PubMed  Google Scholar 

  • Robinson D, Fitter AH (1999) The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. J Exp Bot 50:9–13 doi:10.1093/jexbot/50.330.9

    CAS  Google Scholar 

  • Rochette P, Flanagan LB, Gregorich EG (1999) Separating soil respiration into plant and soil components using analyses of the natural abundance of 13C. Soil Sci Soc Am J 63:1207–1213

    CAS  Google Scholar 

  • Rodger S, Bengough AG, Griffiths BS, Stubbs V, Young IM (2003) Does the presence of detached root border cells of Zea mays alter the activity of the pathogenic nematode Meloidogyne incognita?. Phytopath 93:1111–1114 doi:10.1094/PHYTO.2003.93.9.1111

    CAS  Google Scholar 

  • Roose T, Fowler AC (2004) A mathematical model for water and nutrient uptake by plant root systems. J Theor Biol 228:173–184 doi:10.1016/j.jtbi.2003.12.013

    PubMed  CAS  Google Scholar 

  • Rosling A, Lindahl BD, Finlay RD (2004a) Carbon allocation in intact mycorrhizal systems of Pinus sylvestris L. seedlings colonizing different mineral substrates. New Phytol 162:795–802 doi:10.1111/j.1469-8137.2004.01080.x

    Google Scholar 

  • Rosling A, Lindahl BD, Taylor AFS, Finlay RD (2004b) Mycelial growth and substrate acidification of ectomycorrhizal fungi in response to different minerals. FEMS Microbiol Ecol 47:31–37 doi:10.1016/S0168-6496(03)00222-8

    CAS  PubMed  Google Scholar 

  • Rothe A, Binkley D (2001) Nutritional interactions in mixed species forests: a synthesis. Can J Res 31:1855–1870 doi:10.1139/cjfr-31-11-1855

    Google Scholar 

  • Roux SJ, Steinebrunner I (2007) Extracellular ATP: an unexpected role as a signaller in plants. Trends Plant Sci 11:522–527 doi:10.1016/j.tplants.2007.09.003

    Google Scholar 

  • Rovira AD (1965) Interactions between plant roots and soil microorganisms. Annu Rev Microbiol 19:241–266 doi:10.1146/annurev.mi.19.100165.001325

    PubMed  CAS  Google Scholar 

  • Rovira AD (1969) Plant root exudates. Bot Rev 35:35–59 doi:10.1007/BF02859887

    CAS  Google Scholar 

  • Rovira AD, Foster RC, Martin JK (1979) Note on terminology: origin, nature and nomenclature of the organic materials in the rhizosphere. In: Harley JL, Scott Russell R (eds) The soil–root interface. Academic, London, pp 1–4

    Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Ann Rev Plant Physiol Plant Mol Biol 52:527–560

    CAS  Google Scholar 

  • Sacchi GA, Abruzzese A, Lucchini G, Fiorani F, Cocucci S (2000) Efflux and active re-absorption of glucose in roots of cotton plants grown under saline conditions. Plant Soil 220:1–11 doi:10.1023/A:1004701912815

    CAS  Google Scholar 

  • Samaj J, Read ND, Volkmann D, Menzel D, Baluska F (2005) The endocytic network in plants. Trends Cell Biol 15:425–433 doi:10.1016/j.tcb.2005.06.006

    PubMed  CAS  Google Scholar 

  • Samuels AL, Fernando M, Glass ADM (1992) Immunofluorescent localization of plasma-membrane H+-ATPase in barley roots and effects of K-nutrition. Plant Physiol 99:1509–1514 doi:10.1104/pp.99.4.1509

    PubMed  CAS  Google Scholar 

  • Sapronov DV, Kuzyakov YV (2007) Separation of root and microbial respiration: comparison of three methods. Eurasian Soil Sci 40:775–784 doi:10.1134/S1064229307070101

    Google Scholar 

  • Scheunert I, Topp E, Attar A, Korte F (1994) Uptake pathways of chlorobenzenes in plants and their correlation with n-octanol/water partition-coefficients. Ecotoxicol Environ Saf 27:90–104 doi:10.1006/eesa.1994.1009

    PubMed  CAS  Google Scholar 

  • Scheurwater I, Clarkson DT, Purves JV, van Rijt G, Saker LR, Welschen R, Lambers H (1999) Relatively large nitrate efflux can account for the high specific respiratory costs for nitrate transport in slow-growing grass species. Plant Soil 215:123–134 doi:10.1023/A:1004559628401

    CAS  Google Scholar 

  • Schnepf A, Roose T (2006) Modelling the contribution of arbuscular mycorrhizal fungi to plant phosphate uptake. New Phytol 171:669–682

    PubMed  CAS  Google Scholar 

  • Schraut D, Ullrich CI, Hartung W (2004) Lateral ABA transport in maize roots (Zea mays): visualization by immunolocalization. J Exp Bot 55:1635–1641 doi:10.1093/jxb/erh193

    PubMed  CAS  Google Scholar 

  • Sherson SM, Alford HL, Forbes SM, Wallace G, Smith SM (2003) Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis. J Exp Bot 54:525–531 doi:10.1093/jxb/erg055

    PubMed  CAS  Google Scholar 

  • Shishkova S, Dubrovsky JG (2005) Developmental programmed cell death in primary roots of Sonoran Desert Cactaceae. Am J Bot 92:1590–1594 doi:10.3732/ajb.92.9.1590

    Google Scholar 

  • Shrestha M, Abraham WR, Shrestha PM, Noll M, Conrad R (2008) Activity and composition of methanotrophic bacterial communities in planted rice soil studied by flux measurements, analyses of pmoA gene and stable isotope probing of phospholipid fatty acids. Environ Microbiol 10:400–412 doi:10.1111/j.1462-2920.2007.01462.x

    PubMed  CAS  Google Scholar 

  • Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R (1997) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–582 doi:10.1038/41557

    CAS  Google Scholar 

  • Singh BK, Millard P, Whiteley AS, Murrell JC (2004) Unravelling rhizosphere–microbial interactions: opportunities and limitations. Trends Microbiol 12:386–393 doi:10.1016/j.tim.2004.06.008

    PubMed  CAS  Google Scholar 

  • Singh BK, Naoise N, Ridgway KP, McNicol J, Young JPW, Daniell TJ, Prosser JI, Millard P (2008) Relationship between assemblages of mycorrhizal fungi and bacteria on grass roots. Environ Microbiol 10:534–541 doi:10.1111/j.1462-2920.2007.01474.x

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Srivastava S, Srivastava AK (2007) Hairy root culture for mass-production of high-value secondary metabolites. Crit Rev Biotechnol 27:29–43 doi:10.1080/07388550601173918

    PubMed  CAS  Google Scholar 

  • Staddon PL, Bronk Ramsey C, Ostle N, Ineson P, Fitter AH (2003) Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of 14C. Science 300:1138–1140 doi:10.1126/science.1084269

    PubMed  CAS  Google Scholar 

  • Stewart AM, Frank DA (2008) Short sampling intervals reveal very rapid root turnover in a temperate grassland. Oecologia 157:453–458 doi:10.1007/s00442-008-1088-9

    PubMed  Google Scholar 

  • Stubbs VEC, Standing D, Knox OGG, Killham K, Bengough AG, Griffiths B (2004) Root border cells take up and release glucose-C. Ann Bot (Lond) 93:221–224 doi:10.1093/aob/mch019

    CAS  Google Scholar 

  • Sugiyama A, Shitan N, Yazaki K (2007) Involvement of a soybean ATP-binding cassette—type transporter in the secretion of genistein, a signal flavonoid in legume–rhizobium symbiosis. Plant Physiol 144:2000–2008 doi:10.1104/pp.107.096727

    PubMed  CAS  Google Scholar 

  • Sun Y-P, Unestam T, Lucas SD, Johanson KJ, Kenne L, Finlay RD (1999) Exudation–reabsorption in mycorrhizal fungi, the dynamic interface for interaction with soil and other microorganisms. Mycorrhiza 9:137–144 doi:10.1007/s005720050298

    CAS  Google Scholar 

  • Swinnen J (1994) Rhizodeposition and turnover of root-derived organic material in barley and wheat under conventional and integrated management. Agric Ecosyst Environ 51:115–128 doi:10.1016/0167-8809(94)90038-8

    Google Scholar 

  • Swinnen J, van Veen JA, Merckx R (1995) Root decay and turnover of rhizodeposits in field-grown winter-wheat and spring barley estimated by 14C pulse-labeling. Soil Biol Biochem 27:211–217 doi:10.1016/0038-0717(94)00161-S

    CAS  Google Scholar 

  • Thaler P, Pages L (1998) Modelling the influence of assimilate availability on root growth and architecture. Plant Soil 201:307–320 doi:10.1023/A:1004380021699

    CAS  Google Scholar 

  • Thornton B (2001) Uptake of glycine by non-mycorrhizal Lolium perenne. J Exp Bot 52:1315–1322 doi:10.1093/jexbot/52.359.1315

    PubMed  CAS  Google Scholar 

  • Thornton B, Paterson E, Midwood AJ, Sim A, Pratt SM (2004) Contribution of current carbon assimilation in supplying root exudates of Lolium perenne measured using steady-state 13C labelling. Physiol Plant 120:434–441 doi:10.1111/j.0031-9317.2004.00250.x

    PubMed  CAS  Google Scholar 

  • Todorovic C, Nguyen C, Robin C, Guckert A (2001) Root and microbial involvement in the kinetics of C-14-partitioning to rhizosphere respiration after a pulse labelling of maize assimilates. Plant Soil 228:179–189 doi:10.1023/A:1004830011382

    CAS  Google Scholar 

  • Toljander JF, Artursson V, Paul LR, Jansson JK, Finlay RD (2006) Attachment of different soil bacteria to arbuscular mycorrhizal fungi is determined by hyphal vitality and fungal species. FEMS Microbiol Lett 254:34–40 doi:10.1111/j.1574-6968.2005.00003.x

    PubMed  CAS  Google Scholar 

  • Toljander JF, Paul L, Lindahl BD, Elfstrand M, Finlay RD (2007) Influence of AM fungal exudates on bacterial community structure. FEMS Microbiol Ecol 61:295–304 doi:10.1111/j.1574-6941.2007.00337.x

    PubMed  CAS  Google Scholar 

  • Treseder KK, Turner KM (2007) Glomalin in ecosystems. Soil Sci Soc Am J 71:1257–1266 doi:10.2136/sssaj2006.0377

    CAS  Google Scholar 

  • van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundström U (2005) The carbon we do not see—the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13 doi:10.1016/j.soilbio.2004.06.010

    Google Scholar 

  • Vandenkoornhuyse P, Mahé S, Ineson P, Staddon P, Ostle N, Cliquet J-B, Francez A-J, Fitter AH, Young JPW (2007) Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proc Natl Acad Sci U S A 104:16970–16975 doi:10.1073/pnas.0705902104

    PubMed  CAS  Google Scholar 

  • Verpoorte R, van der Heijden R, Memelink J (2000) Engineering the plant cell factory for secondary metabolite production. Transgenic Res 9:323–343 doi:10.1023/A:1008966404981

    PubMed  CAS  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586 doi:10.1023/A:1026037216893

    CAS  Google Scholar 

  • Wallander H, Nilsson LO, Hagerberg D, Bååth E (2001) Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:752–760 doi:10.1046/j.0028-646x.2001.00199.x

    Google Scholar 

  • Warembourg FR, Kummerow J (1991) Photosynthesis/translocation studies in terrestrial ecosystems. In: Coleman DC, Fry B (eds) Carbon isotope techniques. Academic, London, pp 11–37

    Google Scholar 

  • Watt M, Hugenholtz P, White R, Vinall K (2006) Numbers and locations of native bacteria on field-grown wheat roots quantified by fluorescence in situ hybridization (Fish). Environ Microbiol 8:871–884 doi:10.1111/j.1462-2920.2005.00973.x

    PubMed  Google Scholar 

  • Welbaum GE, Sturz AV, Dong ZM, Nowak J (2007) Managing soil microorganisms to improve productivity of agro-ecosystems. Crit Rev Plant Sci 23:175–193 doi:10.1080/07352680490433295

    Google Scholar 

  • Wen FS, VanEtten HD, Tsaprailis G, Hawes MC (2007) Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 143:773–783 doi:10.1104/pp.106.091637

    PubMed  CAS  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    PubMed  CAS  Google Scholar 

  • Wichern F, Mayer J, Joergensen RG, Muller T (2007) Rhizodeposition of C and N in peas and oats after 13C-15N double labelling under field conditions. Soil Biol Biochem 39:2527–2537 doi:10.1016/j.soilbio.2007.04.022

    CAS  Google Scholar 

  • Williams LE, Lemoine R, Sauer N (2000) Sugar transporters in higher plants—a diversity of roles and complex regulation. Trends Plant Sci 5:283–290 doi:10.1016/S1360-1385(00)01681-2

    PubMed  CAS  Google Scholar 

  • Wright DP, Read DJ, Scholes JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ 21:881–891 doi:10.1046/j.1365–3040.1998.00351.x

    Google Scholar 

  • Wuyts N, Maung ZTZ, Swennen R, De Waele D (2006) Banana rhizodeposition: characterization of root border cell production and effects on chemotaxis and motility of the parasitic nematode Radopholus similis. Plant Soil 283:217–228 doi:10.1007/s11104-006-0013-4

    CAS  Google Scholar 

  • Yeomans CV, Porteous F, Paterson E, Meharg AA, Killham K (1999) Assessment of lux-marked Pseudomonas fluorescens for reporting on organic carbon compounds. FEMS Microbiol Lett 176:79–83 doi:10.1111/j.1574-6968.1999.tb13645.x

    CAS  Google Scholar 

  • Zhang WH, Ryan PR, Tyerman SD (2004) Citrate-permeable channels in the plasma membrane of cluster roots from white lupin. Plant Physiol 136:3771–3783 doi:10.1104/pp.104.046201

    PubMed  CAS  Google Scholar 

  • Zhao XW, Schmitt M, Hawes MC (2000) Species-dependent effects of border cell and root tip exudates on nematode behaviour. Phytopath 90:1239–1245 doi:10.1094/PHYTO.2000.90.11.1239

    CAS  Google Scholar 

  • Zheng J, Sutton JC, Yu H (2000) Interactions among Pythium aphanidermatum, roots, root mucilage, and microbial agents in hydroponic cucumbers. Can J Plant Pathol 22:368–379

    Google Scholar 

  • Zhu T, Rost TL (2000) Directional cell-to-cell communication in the Arabidopsis root apical meristem. III. Plasmodesmata turnover and apoptosis in meristem and root cap cells during four weeks after germination. Protoplasma 213:99–107 doi:10.1007/BF01280510

    Google Scholar 

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Acknowledgements

The authors would like to address special thanks to L. Pagès (INRA, Avignon) for providing simulations from root architecture models.

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Jones, D.L., Nguyen, C. & Finlay, R.D. Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321, 5–33 (2009). https://doi.org/10.1007/s11104-009-9925-0

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