Skip to main content

The Rhizosphere: Molecular Interactions Between Microorganisms and Roots

  • Chapter
  • First Online:
Growth and Defence in Plants

Part of the book series: Ecological Studies ((ECOLSTUD,volume 220))

Abstract

The rhizosphere has a large impact on plant performance in several ways. A stand-specific, more or less high diversity of microorganisms not only supports the plant in the acquisition of water and nutrients, but also modulates its ability to cope with pathogens. This diversity, however, has to be maintained and thus causes a considerable drain of photoassimilates, which are then not available for shoot development. In this chapter, we try to explain why the considerable allocation of carbon to the root system is a “wise” decision by the plant. We thus focus on the function of root-associated bacteria and their relevance for plant growth and development of disease resistance, and deliver data on the molecular basis of the root–fungus symbiosis (mycorrhiza).

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11:107–114

    Google Scholar 

  • Aquino TM, Plassard C (2004) Dynamics of ectomycorrhizal growth and P transfer to the host plant in response to low and high soil P availability. FEMS Microbiol Ecol 48:149–156

    Google Scholar 

  • Artursson V, Finlay RD, Jansson JK (2005) Combined bromodeoxyuridine immunocapture and terminal-restriction fragment length polymorphism analysis highlights differences in the active soil bacterial metagenome due to Glomus mosseae inoculation or plant species. Environ Microbiol 17:1952–1966

    Google Scholar 

  • Badge US, Prasad R, Varma A (2010) Interaction of mycobiont: Piriformospora indica with medicinal plants and plants of economic importance. Afr J Biotechnol 9:9214–9226

    Google Scholar 

  • Bakker PA, Pieterse CM, van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239–243

    PubMed  Google Scholar 

  • Banerjee MR, Chapman SJ, Killham K (1999) Uptake of fertilizer sulfur by maize from soils of low sulfur status as affected by vesicular-arbuscular mycorrhizae. Can J Soil Sci 79:557–559

    CAS  Google Scholar 

  • Barbosa PG (2004) Identifizierung und molekulare Charakterisierung von Phosphataufnahmesystemen des Ektomykorrhizapilzes Amanita muscaria. Dissertation, Eberhard-Karls University, Tuebingen

    Google Scholar 

  • Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778

    PubMed  CAS  Google Scholar 

  • Barriuso J, Pereyra MT, Lucas García JA, Megías M, Gutiérrez Mañero FJ, Ramos B (2005) Screening for putative PGPR to improve establishment of the symbiosis Lactarius deliciosusPinus sp. Microb Ecol 50:82–89

    PubMed  CAS  Google Scholar 

  • Berdy J (2005) Bioactive microbial metabolites: a personal view. J Antibiot 58:1–26

    PubMed  CAS  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13

    PubMed  CAS  Google Scholar 

  • Bertaux J, Schmid M, Chemidlin Prevost-Boure N, Churin JL, Hartmann A, Garbaye J, Frey-Klett P (2003) In situ identification of intracellular bacteria related to Paenibacillus sp. in the mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Appl Environ Microbiol 69:4243–4248

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bertaux J, Schmid M, Hutzler P, Hartmann A, Garbaye J, Frey-Klett P (2005) Occurrence and distribution of endobacteria in the plant-associated mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Environ Microbiol 7:1786–1795

    PubMed  CAS  Google Scholar 

  • Bianciotto V, Genre A, Jargeat P, Lumini E, Bécard G, Bonfante P (2004) Vertical transmission of endobacteria in the arbuscular mycorrhizal fungus Gigaspora margarita through vegetative spore generations. Appl Environ Microbiol 70:3600–3608

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bieleski RL (1973) Phosphate pools, phosphate transport and phosphate availability. Ann Rev Plant Physiol 24:225–252

    CAS  Google Scholar 

  • Blaha D, Prigent-Combaret C, Mirza MS, Moenne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470

    PubMed  CAS  Google Scholar 

  • Blasius D, Feil W, Kottke I, Oberwinkler F (1986) Hartig net structure and formation of fully ensheated ectomycorrhizas. Nord J Bot 6:837–842

    Google Scholar 

  • Bonfante P, Anca J-A (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383

    PubMed  CAS  Google Scholar 

  • Bruce TJ, Pickett JA (2007) Plant defence signalling induced by biotic attacks. Curr Opin Plant Biol 10:387–92

    PubMed  CAS  Google Scholar 

  • Brulé C, Frey-Klett P, Pierrat JC, Courrier S, Gérard F, Lemoine MC, Rousselet JL, Sommer J, Garbaye J (2001) Survival in the soil of the ectomycorrhizal fungus Laccaria bicolor and effect of a mycorrhiza helper Pseudomonas fluorescens. Soil Biol Biochem 33:1683–1694

    Google Scholar 

  • Buee M, Courty PE, Mignot D, Garbaye J (2007) Soil niche effect on species diversity and catabolic activities in an ectomycorrhizal fungal community. Soil Biol Biochem 39:1947–1955

    CAS  Google Scholar 

  • Buee M, Vairelles D, Garbaye J (2005) Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus silvatica) forest subjected to two thinning regimes. Mycorrhiza 15:235–245

    PubMed  Google Scholar 

  • Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci USA 100(Suppl 2):14555–14561

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chalot M, Blaudez D, Brun A (2006) Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci 11:263–266

    PubMed  CAS  Google Scholar 

  • Chamberlain K, Crawford DL (1999) In vitro and vivo antagonism of pathogenic turfgrass fungi by Streptomyces hygroscopicus strains YCED9 and WYE53. J Ind Microbiol Biotechnol 23:641–646

    PubMed  CAS  Google Scholar 

  • Chen XH, Koumoutsi A, Scholz R, Schneider K, Vater J, Süssmuth R, Piel J, Borriss R (2009a) Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol 140:27–37

    PubMed  CAS  Google Scholar 

  • Chen XH, Scholz R, Borriss M, Junge H, Mögel G, Kunz S, Borriss R (2009b) Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J Biotechnol 140:38–44

    PubMed  CAS  Google Scholar 

  • Cocito C, Di Giambattista M, Nyssen E, Vannuffel P (1997) Inhibition of protein synthesis by streptogramins and related antibiotics. J Antimicrob Chemother 39:7–13

    PubMed  CAS  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959

    PubMed  CAS  PubMed Central  Google Scholar 

  • Conn VM, Walker AR, Franco CM (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21:208–18

    PubMed  CAS  Google Scholar 

  • Conrath U (2006) Systemic acquired resistance. Plant Signal Behav 1:179–184

    PubMed  PubMed Central  Google Scholar 

  • Conrath U, Pieterse CM, Mauch-Mani B (2002) Priming in plant-pathogen interactions. Trends Plant Sci 7:210–16

    PubMed  CAS  Google Scholar 

  • Cooley M, Chhabra SR, Williams P (2008) N-Acylhomoserine lactone-mediated quorum sensing: a twist in the tail and a blow for host immunity. Chem Biol 15:1141–1147

    PubMed  CAS  Google Scholar 

  • Coombs JT, Franco CM (2003) Isolation and identification of actinobacteria from surface-sterilized wheat roots. Appl Environ Microbiol 69:5603–5608

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cornelis P, Matthijs S (2002) Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdins. Environ Microbiol 4:787–798

    PubMed  CAS  Google Scholar 

  • Corratge C, Zimmermann S, Lambilliotte R, Plassard C, Marmeisse R, Thibaud JB, Lacombe B, Sentenac H (2007) Molecular and functional characterization of a Na+-K+ transporter from the Trk family in the ectomycorrhizal fungus Hebeloma cylindrosporum. J Biol Chem 282:26057–26066

    PubMed  CAS  Google Scholar 

  • Courty P-E, Breda N, Garbaye J (2007) Relation between oak tree phenology and the secretion of organic matter degrading enzymes by Lactarius quietus ectomycorrhizas before and during bud break. Soil Biol Biochem 39:1655–1663

    CAS  Google Scholar 

  • Courty P-E, Pritsch K, Schloter M, Hartmann A, Garbaye J (2005) Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytol 167:309–319

    PubMed  CAS  Google Scholar 

  • Couturier J, Montanini B, Martin F, Brun A, Blaudez D, Chalot M (2007) The expanded family of ammonium transporters in the perennial poplar plant. New Phytol 174:137–150

    PubMed  CAS  Google Scholar 

  • Crawford DL, Lynch JM, Whipps JM, Ousley MA (1993) Isolation and characterization of actinomycete antagonists of a fungal root pathogen. Appl Environ Microbiol 59:3899–3905

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Loucao MA, Jakobsen I (2007) Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144:782–792

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cui J, Bahrami AK, Pringle EG, Hernandez-Guzman G, Bender CL, Pierce NE, Ausübel FM (2005) Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc Natl Acad Sci USA 102:1791–96

    PubMed  CAS  PubMed Central  Google Scholar 

  • Davelos AL, Kinkel LL, Samac DA (2004) Spatial variation in frequency and intensity of antibiotic interactions among Streptomycetes from prairie soil. Appl Environ Microbiol 70:1051–58

    PubMed  CAS  PubMed Central  Google Scholar 

  • De Almeida CV, Andreote FD, Yara R, Tanaka FAO, Azevedo JL, de Almeida M (2009) Bacteriosomes in axenic plants: endophytes as stable endosymbionts. World J Microbiol Biotechnol. doi:10.1007/s11274-009-0073-8

  • Delalande L, Faure D, Raffoux A, Uroz S, D’Angelo-Picard C, Elasri M, Carlier A, Berruyer R, Petit A, Williams P, Dessaux Y (2005) N-hexanoyl-L-homoserine lactone, a mediator of bacterial quorum-sensing regulation, exhibits plant-dependent stability and may be inactivated by germinating Lotus corniculatus seedlings. FEMS Microbiol Ecol 52:13–20

    PubMed  CAS  Google Scholar 

  • Deveau A, Kohler A, Frey-Klett P, Martin F (2008) The major pathways of carbohydrate metabolism in the ectomycorrhizal basidiomycete Laccaria bicolor S238N. New Phytol 180:379–390

    PubMed  CAS  Google Scholar 

  • Deveau A, Palin B, Delaruelle C, Peter M, Kohler A, Pierrat JC, Sarniguet A, Garbaye J, Martin F, Frey-Klett P (2007) The mycorrhizal helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytol 175:743–755

    PubMed  CAS  Google Scholar 

  • Dobbelaere S, Croonenborghs A, Amber T, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguiire JF, Kapulnik Y, Shimon B, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:871–879

    Google Scholar 

  • Dobbelaere S, Okon Y (2007) The plant growth-promoting effect and plant responses. In: Elmerich C, Newton WE (eds) Associative and endophytic nitrogen-fixing bacteria and cyanonbacterial associations. Springer, Dordrecht, pp 145–170

    Google Scholar 

  • Dunne C, Moenne-Loccoz Y, de Bruijn F, O’Gara F (2000) Overproduction of an inducible extracellular serine protease improves biological control of Pythium ultimum by Stenotrophomonas maltophilia strain W81. Microbiology 146:2069–2078

    PubMed  CAS  Google Scholar 

  • Duplessis S, Courty PE, Tagu D, Martin F (2005) Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol 165:599–611

    PubMed  CAS  Google Scholar 

  • Eberl L (1999) N-Acyl homoserine lactone-mediated gene regulation in Gram-negative bacteria. Syst Appl Microbiol 22:493–506

    PubMed  CAS  Google Scholar 

  • Eckwall EC, Schottel JL (1997) Isolation and characterization of an antibiotic produced by the scab disease-suppressive Streptomyces diastatochromogenes strain PonSSII. J Ind Microbiol Biotechnol 19:220–225

    PubMed  CAS  Google Scholar 

  • El-Abyad MS, El-Sayed MA, El-Shanshoury AR, El-Sabbagh SM (1993) Towards the biological control of fungal and bacterial diseases of tomato using antagonistic Streptomyces spp. Plant Soil 149:185–195

    Google Scholar 

  • Fajardo Lopez M, Dietz S, Grunze N, Bloschies J, Weiss M, Nehls U (2008) The sugar porter gene family of Laccaria bicolor: function in ectomycorrhizal symbiosis and soil-growing hyphae. New Phytol 180:365–378

    Google Scholar 

  • Fajardo López M, Männer P, Willmann A, Hampp R, Nehls U (2007) Increased trehalose biosynthesis in Hartig net hyphae of ectomycorrhizas. New Phytol 74:389–398

    Google Scholar 

  • Fiedler HP, Krastel P, Muller J, Gebhardt K, Zeeck A (2001) Enterobactin: the characteristic catecholate siderophore of Enterobacteriaceae is produced by Streptomyces species. FEMS Microbiol Lett 196:147–151

    PubMed  CAS  Google Scholar 

  • Firn RD, Jones CG (2000) The evolution of secondary metabolism – a unifying model. Mol Microbiol 37:989–994

    PubMed  CAS  Google Scholar 

  • Frey-Klett P, Chavarte M, Clausse ML, Courrier S, Le Roux C, Raaijmakers J, Martinotti M, Pierrat JC, Garbaye J (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165:317–328

    PubMed  Google Scholar 

  • Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    PubMed  CAS  Google Scholar 

  • Galagan JE, Henn MR, Ma L-J, Cuomo CA, Birren B (2005) Genomics of the fungal kingdom: insights into eukaryotic biology. Genome Res 15:1620–1631

    PubMed  CAS  Google Scholar 

  • Gantner S, Schmid M, Dürr C, Schuhegger R, Steidle A, Hutzler P, Langebartels C, Eberl L, Hartmann A, Dazzo FB (2006) In situ spatial scale of calling distances and population density-independent N-Acylhomoserine lactone mediated communication by rhizobacteria colonized on plant roots. FEMS Microbiol Ecol 56:188–194

    PubMed  CAS  Google Scholar 

  • Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J Theor Biol 190:63–68

    PubMed  CAS  Google Scholar 

  • Götz C, Fekete A, Gebefuegi I, Forczek S, Fuksová K, Li X, Englmann M, Gryndler M, Hartmann A, Matucha M, Schmitt-Kopplin P, Schröder P (2007) Uptake, degradation and chiral discrimination of N -acyl-D/L-homoserine lactones by barley (Hordeum vulgare) and yam bean (Pachyrhizus erosus) plants. Anal Bioanal Chem 389:1447–1457

    PubMed  Google Scholar 

  • Gray LE, Gerdemann JW (1972) Uptake of sulphur-35 by vesicular-arbuscular mycorrhizae. Plant Soil 39:687–698

    Google Scholar 

  • Grichko VP, Glick BR (2001) Ameloriation of flooding stress by ACC deaminase-containing plant growth production. Plant Physiol Biochem 39:11–18

    CAS  Google Scholar 

  • Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319

    PubMed  CAS  Google Scholar 

  • Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14

    CAS  Google Scholar 

  • Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–255

    CAS  Google Scholar 

  • Hense BA, Kuttler C, Mueller J, Rothballer M, Hartmann A, Kreft J-U (2007) Does efficiency sensing unify diffusion and quorum sensing? Nat Rev Microbiol 5:230–239

    PubMed  CAS  Google Scholar 

  • Herschbach C, Rennenberg H (1994) Influence of glutathione (gsh) on net uptake of sulphate and sulphate transport in tobacco plants. J Exp Bot 45:1069–1076

    CAS  Google Scholar 

  • Hiltner L (1904) Über neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie unter besonderer Berücksichtigung der Gründüngung und Brache. Arb Dtsch Landw Ges 98:59–78

    Google Scholar 

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

    CAS  Google Scholar 

  • Hogan DA, Vik A, Kolter R (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54:1212–1223

    PubMed  CAS  Google Scholar 

  • Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Env Microbiol 72:1719–28

    CAS  Google Scholar 

  • Jany JL, Martin F, Garbaye J (2003) Respiration activity of ectomycorrhizas from Cenococcum geophilum and Lactarius sp. in relation to soil water potential in five beech forests. Plant Soil 255:487–494

    CAS  Google Scholar 

  • Jargeat P, Cosseau C, Ola’h B, Jauneau A, Bonfante P, Batut J, Bécard G (2004) Isolation, free-living capacities and genome structure of Candidatus Glomeribacter gigasporarum, the endocellular bacteria of the mycorrhizal fungus Gigaspora margarita. J Bacteriol 186:6876–6884

    PubMed  CAS  PubMed Central  Google Scholar 

  • Johansson T, Le Quèrè A, Ahren D, Söderström B, Erlandsson R, Lundeberg J, Uhlen M, Tunlid A (2004) Transcriptional responses of Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. Mol Plant Microb Interact 17:202–215

    Google Scholar 

  • Kemppainen M, Duplessis S, Martin F, Pardo AG (2008) T-DNA insertion, plasmid rescue and integration analysis in the model mycorrhizal fungus Laccaria bicolor. Microb Biotechnol 1:258–269

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286:885–886

    CAS  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    PubMed  CAS  Google Scholar 

  • Kottke I, Oberwinkler F (1987) The cellular structure of the Hartig net: coenocytic and transfer cell-like organization. Nord J Bot 7:85–95

    Google Scholar 

  • Koumoutsi A, Chen X-H, Henne A, Liesegang H, Hitzeroth G, Franke P, Vater J, Borriss R (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186:1084–1096

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kowallik W, Thiemann M, Huang Y, Mutumba G, Beermann L, Broer D, Grotjohann N (1998) Complete sequence of glycolytic enzymes in the mycorrhizal basidiomycete, Suillus bovinus. Z Naturforsch 53:818–827

    CAS  Google Scholar 

  • Kredich NM (1993) Gene regulation of sulfur assimilation. In: DeKok LJ, Stulen I, Rennenberg H, Brunold C, Rauser WE (eds) Sulfur nutrition and sulfur assimilation in higher plants. SPB, The Hague, pp 61–76

    Google Scholar 

  • Kreuzwieser J, Herschbach C, Rennenberg H (1996) Sulphate uptake and xylem loading of non-mycorrhizal excised roots of young beech (Fagus sylvatica) trees. Plant Physiol Biochem 34:409–416

    CAS  Google Scholar 

  • Kreuzwieser J, Rennenberg H (1998) Sulphate uptake and xylem loading of mycorrhizal beech roots. New Phytol 140:319–329

    CAS  Google Scholar 

  • Küster H, Becker A, Firnhaber C, Hohnjec N, Manthey K, Perlick AM, Bekel T, Dondrup M, Henckel K, Goesmann A, Meyer F, Wipf D, Requena N, Hildebrandt U, Hampp R, Nehls U, Krajinski F, Franken P, Pühler A (2007) Development of bioinformatic tools to support EST-sequencing, in silico- and microarray-based transcriptome profiling in mycorrhizal symbioses. Phytochemistry 68:19–32

    PubMed  Google Scholar 

  • Lappartient AG, Vidmar JJ, Leustek T, Glass ADM, Touraine B (1999) Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J 18:89–95

    PubMed  CAS  Google Scholar 

  • Laurent P, Voiblet C, Tagu D, de Carvalho D, Nehls U, De Bellis R, Balestrini R, Bauw G, Bonfante P, Martin F (1999) A novel class of ectomycorrhiza-regulated cell wall polypeptides in Pisolithus tinctorius. Mol Plant Microb Interact 12:862–871

    CAS  Google Scholar 

  • Le Quere A, Wright D, Soederstroem B, Tunlid A, Johansson T (2005) Global patterns of gene regulation associated with the development of ectomycorrhiza between birch (Betula pendula roth.) and Paxillus involutus (batsch) Fr. Mol Plant Microb Interact 18:659–673

    Google Scholar 

  • Lehr NA, Schrey SD, Bauer R, Hampp R, Tarkka MT (2007) Suppression of plant defence response by a mycorrhiza helper bacterium. New Phytol 174:892–903

    PubMed  CAS  Google Scholar 

  • Lehr NA, Schrey SD, Hampp R, Tarkka MT (2008) Root inoculation with a forest soil streptomycete leads to locally and systemically increased resistance against phytopathogens in Norway spruce. New Phytol 177:965–76

    PubMed  Google Scholar 

  • Leveau JHJ, Gerards S (2008) Discovery of a bacterial gene cluster for catabolism of the plant hormone indole-3-acetic acid. FEMS Microbiol Ecol 65:238–250

    PubMed  CAS  Google Scholar 

  • Liras P (1999) Biosynthesis and molecular genetics of cephamycins. Cephamycins produced by actinomycetes. Antonie Leeuwenhoek 75:109–124

    PubMed  CAS  Google Scholar 

  • Liu D, Anderson NA, Kinkel LL (1995) Biological control of potato scab in the field with antagonistic Streptomyces scabies. Phytopathology 85:827–831

    Google Scholar 

  • Loria R, Bukhalid RA, Fry BA, King RR (1997) Plant pathogenicity in the genus Streptomyces. Plant Dis 81:836–846

    Google Scholar 

  • Loria R, Kers J, Joshi M (2006) Evolution of plant pathogenicity in Streptomyces. Annu Rev Phytopathol 44:469–87

    PubMed  CAS  Google Scholar 

  • Lucic E, Fourrey C, Kohler A, Martin F, Chalot M, Brun-Jacob A (2008) A gene repertoire for nitrogen transporters in Laccaria bicolor. New Phytol 180:343–364

    PubMed  CAS  Google Scholar 

  • Lucy M, Reed E, Glick BR (2004) Application of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek 86:1–25

    PubMed  CAS  Google Scholar 

  • Lumini E, Ghignone S, Bianciotto V, Bonfante P (2007) Endobacteria or bacterial symbionts? To be or not to be. New Phytol 170:205–208

    Google Scholar 

  • Maier A, Riedlinger J, Fiedler H-P, Hampp R (2004) Actinomycetales bacteria from a spruce stand: characterization and effects on growth of root symbiotic, and plant parasitic soil fungi in dual culture. Mycol Progr 3:129–36

    Google Scholar 

  • Mansouri-Bauly H, Sýkorová Z, Scheerer U, Kopriva S (2006) Sulfur uptake in the ectomycorrhizal fungus Laccaria bicolor S238N. Mycorrhiza 16:421–427

    PubMed  CAS  Google Scholar 

  • Marilley L, Hartwig UA, Aragno M (1999) Influence of an elevated atmospheric CO2 content on soil and rhizosphere bacterial communities beneath Lolium perenne and Trifolium repens under field conditions. Microb Ecol 38:39–49

    PubMed  CAS  Google Scholar 

  • Martin F, Aerts A, Ahrén D, Brun A, Duchaussoy F, Kohler A, Lindquist E, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Danchin EGJ, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Gibon J, Grimwood J, Hoegger P, Jain P, Kilaru S, Labbé J, Lin Y, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Pereda V, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kües U, Lucas S, Van de Peer Y, Podila G, Polle A, Pukkila PJ, Richardson PM, Rouzé P, Sanders I, Stajich JE, Tunlid A, Tuskan G, Grigoriev I (2008) The genome sequence of the basidiomycete fungus Laccaria bicolor provides insights into the mycorrhizal symbiosis. Nature 452:88–92

    PubMed  CAS  Google Scholar 

  • Martin F, Canet D, Marchal JP (1985) 13C nuclear magnetic resonance study of mannitol cycle and trehalose synthesis during glucose utilization by the ectomycorrhizal ascomycete Cenococcum geophilum. Plant Physiol 77:499–502

    PubMed  CAS  PubMed Central  Google Scholar 

  • Martin F, Nehls U (2009) Harnessing ectomycorrhizal genomics for ecological insights. Curr Opin Plant Biol 12:508–515

    PubMed  CAS  Google Scholar 

  • Martin F, Tunlid A (2009) The ectomycorrhizal symbiosis: a marriage of convenience. In: Deising HB (ed) The mycota, vol V, 2nd edn, Plant relationships. Springer, Heidelberg, pp 237–257

    Google Scholar 

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

    CAS  Google Scholar 

  • Menotta M, Amicucci A, Sisti D, Gioacchini AM, Stocchi V (2004) Differential gene expression during pre-symbiotic interaction between Tuber borchii vittad. and Tilia americana l. Curr Genet 46:158–165

    PubMed  CAS  Google Scholar 

  • Morel M, Jacob C, Fitz M, Wipf D, Chalot M, Brun A (2008) Characterization and regulation of PiDur3, a permease involved in the acquisition of urea by the ectomycorrhizal fungus Paxillus involutus. Fungal Genet Biol 45:912–921

    PubMed  CAS  Google Scholar 

  • Morel M, Jacob J, Kohler A, Johansson A, Martin F, Chalot M, Brun A (2005) Identification of genes differentially expressed in extraradical mycelium and ectomycorrhizal roots during Paxillus involutus-Betula pendula ectomycorrhizal symbiosis. Appl Environ Microbiol 71:382–391

    PubMed  CAS  PubMed Central  Google Scholar 

  • Morgan JAW, Morgan G, Bending D, White PJ (2005) Biological costs and benefits to plant–microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739

    PubMed  CAS  Google Scholar 

  • Müller T, Avolio M, Olivi M, Benjdia M, Rikirsch E, Kasaras A, Fitz M, Chalot M, Wipf D (2007) Nitrogen transport in the ectomycorrhiza association: the Hebeloma cylindrosporum-Pinus pinaster model. Phytochemistry 68:41–51

    PubMed  Google Scholar 

  • Nabti E, Sahnoune M, Adjrad S, Van Dommelen A, Ghoul M, Schmid M, Hartmann A (2007) A halophilic and osmotolerant Azospirillum brasilense strain from Algerian soil restores wheat growth under saline conditions. Eng Life Sci 7:354–360

    CAS  Google Scholar 

  • Nabti E, Sahnoune M, Ghoul M, Fischer D, Hofmann A, Rothballer M, Schmid M, Hartmann A (2010) Restoration of growth of durum wheat (Triticum durum var. waha) under saline conditions due to inoculation with the rhizosphere bacterium Azospirillum brasilense NH and extracts of the marine alga Ulva lactuca. J Plant Growth Regul 29:6–22

    CAS  Google Scholar 

  • Nakayama T, Homma Y, Hashidoko Y, Mitzutani J, Tahara S (1999) Possible role of xanthobaccins produced by Stenotrophomonas sp. strain SB-K88 in suppression of sugar beet damping-off disease. Appl Environ Microbiol 65:4334–4339

    PubMed  CAS  PubMed Central  Google Scholar 

  • Neeno-Eckwall EC, Kinkel LL, Schottel JL (2001) Competition and antibiosis in the biological control of potato scab. Can J Microbiol 47:332–340

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nehls U, Grunze N, Willmann M, Reich M, Küster H (2007) Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phytochemistry 68:82–91

    PubMed  CAS  Google Scholar 

  • Nuutinen JT, Timonen S (2008) Identification of nitrogen mineralization enzymes, l-amino acid oxidases, from the ectomycorrhizal fungi Hebeloma spp. and Laccaria bicolor. Mycol Res 112:1453–1464

    PubMed  CAS  Google Scholar 

  • Nygren CMR, Eberhardt U, Karlsson M, Parrent JL, Lindahl BD, Taylor AFS (2008) Growth on nitrate and occurrence of nitrate reductase-encoding genes in a phylogenetically diverse range of ectomycorrhizal fungi. New Phytol 180:875–889

    PubMed  CAS  Google Scholar 

  • Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformopsora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–18

    Google Scholar 

  • Ongena M, Jourdan E, Schäfer M, Kech C, Budzikiewicz H, Luxen A, Thonart P (2005) Isolation of an N-alkylated benzylamine derivative from Pseudomonas putida BTP1 as elicitor of induced systemic resistance in bean. Mol Plant Microbe Interact 18:562–569

    PubMed  CAS  Google Scholar 

  • Ono BI, Hazu T, Yoshida S, Kawato T, Shinoda S, Brzvwczy J, Paszewski A (1999) Cysteine biosynthesis in Saccharomyces cerevisiae: a new outlook on pathway and regulation. Yeast 15:1365–1375

    PubMed  CAS  Google Scholar 

  • Opelt K, Berg G (2004) Diversity and antagonistic potential of bacteria associated with bryophytes from nutrient-poor habitats of the baltic sea coast. Appl Environ Microbiol 70:6569–6579

    PubMed  CAS  PubMed Central  Google Scholar 

  • Peter M, Courty P, Kohler A, Delaruelle C, Martin D, Tagu D, Frey-Klett P, Duplessis S, Chalot M, Podila G, Martin F (2003) Analysis of expressed sequence tags from the ectomycorrhizal basidiomycetes Laccaria bicolor and Pisolithus microcarpus. New Phytol 159:117–129

    CAS  Google Scholar 

  • Pieterse MJC, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:309–316

    Google Scholar 

  • Prigent-Combaret C, Blaha D, Pothier JF, Vial L, Poirier M-A, Wisniewski-Dyé F, Moenne-Loccoz Y (2008) Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the 1-aminocyclooropane-1-carboxylate deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other Proteobacteria. FEMS Microbiol Ecol 65:202–219

    PubMed  CAS  Google Scholar 

  • Pritsch K, Raidl S, Marksteiner E, Blaschke H, Agerer R, Schloter M, Hartmann A (2004) A rapid and highly sensitive method for measuring enzyme activities in single mycorrhizal tips using 4-methylumbelliferonelabelled fluorogenic substrates in a microplate system. J Microbiol Methods 58:233–241

    PubMed  CAS  Google Scholar 

  • Raaijmakers JM, Vlami M, de Souza JT (2002) Antibiotic production by bacterial biocontrol agents. Antonie van Leeuwenhoek 81:537–547

    PubMed  CAS  Google Scholar 

  • Riedlinger J, Schrey SD, Tarkka MT, Hampp R, Kapur M, Fiedler H-P (2006) Auxofuran, a novel metabolite stimulating growth of fly agaric, produced by the mycorrhiza helper bacterium Streptomyces AcH 505. Appl Environ Microbiol 72:3550–3557

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837

    PubMed  CAS  Google Scholar 

  • Rothballer M, Schmid M, Hartmann A (2009) Diazotrophic bacterial endophytes in Gramineae and other plants. In: Pawlowski K (ed) Prokaryotic symbionts in plants, vol 8, Microbiol monographs. Springer, Heidelberg, pp 273–302

    Google Scholar 

  • Rovira AD (1991) Rhizosphere research – 85 years of progress and frustration. In: Kleister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer, Amsterdam, pp 3–13

    Google Scholar 

  • Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Sci Acad USA 100:4927–4932

    CAS  Google Scholar 

  • Samac DA, Kinkel LL (2001) Suppression of the root-lesion nematode (Pratylenchus penetrans) in alfalfa (Medicago sativa) by Streptomyces spp. Plant Soil 235:35–44

    CAS  Google Scholar 

  • Saravesi K, Markkola A, Rautio P, Roitto M, Tuomi J (2008) Defoliation causes parallel temporal responses in a host tree and its fungal symbionts. Oecologia 156:117–123

    PubMed  Google Scholar 

  • Sardi P, Saracchi M, Quaroni S, Petrolini B, Borgonovi GE, Merli S (1992) Isolation of endophytic Streptomyces strains from surface-sterilized roots. Appl Environ Microbiol 58:2691–93

    PubMed  CAS  PubMed Central  Google Scholar 

  • Schaefer AL, Greenberg EP, Oliver CM, Oda Y, Huang JJ, Bittan-Banin G, Peres CM, Schmidt S, Juhaszova K, Sufrin JR, Harwood CS (2008) A new class of homoserine lactone quorum-sensing signals. Nature 454:595–599

    PubMed  CAS  Google Scholar 

  • Schertzer JW, Boulette ML, Whiteley M (2009) More than a signal: non-signaling properties of quorum sensing molecules. Trends Microbiol 17:189–195

    PubMed  CAS  Google Scholar 

  • Schottel JL, Shimizu K, Kinkel LL (2001) Relationships of in vitro pathogen inhibition and soil colonization to potato scab biocontrol by antagonistic Streptomyces spp. Biol Control 20:102–112

    Google Scholar 

  • Schrey SD, Schellhammer M, Ecke M, Hampp R, Tarkka MT (2005) Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205–216

    PubMed  CAS  Google Scholar 

  • Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler P, Schmid M, van Breusegem F, Eberl L, Hartmann A, Langebartels C (2006) Induction of systemic resistance in tomato by N-acylhomoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29:909–918

    PubMed  CAS  Google Scholar 

  • Seegmüller S, Schulte M, Herschbach C, Rennenberg H (1996) Interactive effects of mycorrhization and elevated atmospheric CO2 on sulphur nutrition of young pedunculate oak (Quercus robur l.) trees. Plant Cell Environ 19:418–426

    Google Scholar 

  • Selle A, Willmann M, Grunze N, Geßler A, Weiß M, Nehls U (2005) The high-affinity poplar ammonium importer PttAmt1.2 and its role in ectomycorrhizal symbiosis. New Phytol 168:697–706

    PubMed  CAS  Google Scholar 

  • Selosse MA, Setaro S, Glatard F, Richard F, Urcelay C, Weiss M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878

    PubMed  CAS  Google Scholar 

  • Sharma M, Schmid M, Rothballer M, Hause G, Zuccaro A, Imani J, Schäfer P, Hartmann A, Kogel K-H (2008) Detection and identification of mycorrhiza helper bacteria intimately associated with representatives of the order Sebacinales. Cell Microbiol 10:2235–2246

    PubMed  CAS  Google Scholar 

  • Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Roskot N, Heuer H, Berg B (2001) Bulk and rhizosphere bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751

    PubMed  CAS  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, Oxford, UK

    Google Scholar 

  • Soanes DM, Alam I, Cornell M, Wong HM, Hedeler C, Paton NW, Rattray M, Hubbard SJ, Oliver SG, Talbot NJ (2008) Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS One 3(6):e2300. doi:10.1371/journal.pone.0002300

    PubMed  PubMed Central  Google Scholar 

  • Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506

    PubMed  CAS  Google Scholar 

  • Sugarawa M, Okazaki S, Nukui N, Ezura H, Mitsui H, Minamisawa K (2006) Rhizobitoxin modulates plant microbe interactions by ethylene inhibition. Biotechnol Adv 24:382–388

    Google Scholar 

  • Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963

    Google Scholar 

  • Tarkka M, Nehls U, Hampp R (2005) Physiology of ectomycorrhiza (ECM). In: Lüttge U (ed) Progress in botany. Springer, Berlin, pp 247–276

    Google Scholar 

  • Tarkka MT, Hampp R (2008) Secondary metabolites of soil streptomycetes in biotic interactions. In: Karlovsky P (ed) Secondary metabolites in soil ecology, vol 14, Soil biology series. Springer, Berlin, pp 107–28

    Google Scholar 

  • Tatry MV, Kassis EE, Lambilliotte R, Corratgé C, van Aarle I, Amenc LK, Alary R, Zimmermann S, Sentenac H, Plassard C (2008) Two differentially regulated phosphate transporters from the symbiotic fungus Hebeloma cylindrosporum and phosphorus acquisition by ectomycorrhizal Pinus pinaster. Plant J 57:1092–1102

    PubMed  Google Scholar 

  • van Aarle I, Viennois G, Amenc LK, Tatry MV, Luu D, Plassard C (2007) Fluorescent in situ rt-PCR to visualise the expression of a phosphate transporter gene from an ectomycorrhizal fungus. Mycorrhiza 17:487–494

    PubMed  Google Scholar 

  • Van de Kamp M, Schuurs TA, Vos A, Van der Lende TR, Konings WN, Driessen AJM (2000) Sulfur regulation of the sulfate transporter genes Suta and Sutb in Penicillium chrysogenum. Appl Env Microbiol 66:4536–4538

    Google Scholar 

  • Vance C, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    CAS  Google Scholar 

  • Verma SA, Varma A, Rexer KH, Hassel A, Kost G, Sabhoy A, Bisen P, Bütehorn B, Franken P (1998) Piriformospora indica, gen. et spec. nov., a new root-colonizing fungus. Mycologia 90:898–905

    Google Scholar 

  • von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, Hartmann A, Schmitt-Kopplin P, Durner J (2008) The response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229:73–85

    CAS  Google Scholar 

  • von Rad U, Mueller MJ, Durner J (2005) Evaluation of natural and synthetic stimulants of plant immunity by microarray technology. New Phytol 165:191–202

    Google Scholar 

  • Weissman KJ, Leadlay PF (2005) Combinatorial biosynthesis of reduced polyketides. Nat Rev Microbiol 3:925–936

    PubMed  CAS  Google Scholar 

  • Weller DM (1988) Biological control of soilborne pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407

    Google Scholar 

  • Weller DM, Raaijmakers JM, Gardener BB, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348

    PubMed  CAS  Google Scholar 

  • Westerman S, Stulen I, Suter M, Brunold C, De Kok LJ (2001) Atmospheric H2S as sulphur source for Brassica oleracea: consequences for the activity of the enzymes of the assimilatory sulphate reduction pathway. Plant Physiol Biochem 39:425–432

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Wiemken V (2007) Trehalose synthesis in ectomycorrhizas – a driving force of carbon gain for fungi? New Phytol 174:228–230

    PubMed  CAS  Google Scholar 

  • Wiener P (2000) Antibiotic production in a spatially structured environment. Ecol Lett 3:122–133

    Google Scholar 

  • Willmann A, Weiss M, Nehls U (2007) Ectomycorrhiza-mediated repression of the high-affinity ammonium importer gene Am Amt2 in Amanita muscaria. Curr Genet 51:71–78

    PubMed  CAS  Google Scholar 

  • Woo JH, Kitamura E, Myuoga H, Yuto K (2002) An antifungal protein from the marine bacterium Streptomyces sp. strain AP77 is specific for Pythium porphyrae, a causative agent of red rot disease in Porphyra spp. Appl Environ Microbiol 68:2666–2675

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wright DP, Johansson T, Le Quere A, Soderstrom B, Tunlid A (2005) Spatial patterns of gene expression in the extramatrical mycelium and mycorrhizal root tips formed by the ectomycorrhizal fungus Paxillus involutus in association with birch (Betula pendula) seedlings in soil microcosms. New Phytol 167:579–596

    PubMed  CAS  Google Scholar 

  • Xiao K, Samac DA, Kinkel LL (2002) Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biol Control 23:285–95

    CAS  Google Scholar 

  • Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

As far as own research has been addressed, financial support by the Deutsche Forschungsgemeinschaft is gratefully acknowledged. We are indebted to Nina Lehr, Silvia Schrey, and Mika Tarkka for their input, and to Reinhard Agerer for critical reading and many helpful suggestions. GB 4-2 was isolated by K. Poralla (University of Tübingen).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Hampp .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Hampp, R., Hartmann, A., Nehls, U. (2012). The Rhizosphere: Molecular Interactions Between Microorganisms and Roots. In: Matyssek, R., Schnyder, H., Oßwald, W., Ernst, D., Munch, J., Pretzsch, H. (eds) Growth and Defence in Plants. Ecological Studies, vol 220. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30645-7_5

Download citation

Publish with us

Policies and ethics