Skip to main content
SpringerLink
Log in

Role of Proteins Secreted by Rhizobia in Symbiotic Interactions with Leguminous Roots

  • Chapter
Microbial Root Endophytes

Part of the book series: Soil Biology ((SOILBIOL,volume 9))

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Atkins CA, Ritchie A, Rowe PB, McCairns E, Sauer D (1982) De novo purine synthesis in nitrogen-fixing nodules of cowpea (Vigna unguiculata [L.] Walp.) and soybean (Glycine max [L.] Merr.). Plant Physiol 70:55–60

    PubMed  CAS  Google Scholar 

  • Bartsev AV, Boukli NM, Deakin WJ, Staehelin C, Broughton WJ (2003) Purification and phosphorylation of the effector protein NopL from Rhizobium sp. NGR234. FEBS Lett 554:271–274

    Article  PubMed  CAS  Google Scholar 

  • Bartsev AV, Deakin WJ, Boukli NM, McAlvin CB, Stacey G, Malnöe P, Broughton WJ, Staehelin C (2004a) NopL, an effector protein of Rhizobium sp. NGR234, thwarts activation of plant defense reactions. Plant Physiol 134:871–879

    Article  PubMed  CAS  Google Scholar 

  • Bartsev AV, Kobayashi H, Broughton WJ (2004b) Rhizobial signals convert pathogens to symbionts at the legume interface. In: Gillings M, Holmes A (eds) Plant microbiology, Bios Scientific, Oxfordshire, UK, pp 19–28

    Google Scholar 

  • Becker A, Ruberg S, Kuster H, Roxlau AA, Keller M, Ivashina T, Cheng HP, Walker GC, Pühler A (1997) The 32-kilobase exp gene cluster of Rhizobium meliloti directing the biosynthesis of galactoglucan: genetic organization and properties of the encoded gene products. J Bacteriol 179:1375–1384

    PubMed  CAS  Google Scholar 

  • Broughton WJ, Jabbouri S, Perret X (2000) Keys to symbiotic harmony. J Bacteriol 182:5641–5652

    Article  PubMed  CAS  Google Scholar 

  • Büttner D, Nennstiel D, Klusener B, Bonas U (2002) Functional analysis of HrpF, a putative type III translocon protein from Xanthomonas campestris pv. vesicatoria. J Bacteriol 184:2389–2398

    Article  PubMed  CAS  Google Scholar 

  • Christie PJ (1997) Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria. J Bacteriol 179:3085–3094

    PubMed  CAS  Google Scholar 

  • Christie PJ (2001) Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol Microbiol 40:294–305

    Article  PubMed  CAS  Google Scholar 

  • De Maagd RA, Wijfjes AH, Spaink HP, Ruiz-Sainz JE, Wijffelman CA, Okker RJ, Lugtenberg BJ (1989) nodO, a new nod gene of the Rhizobium leguminosarum biovar viciae sym plasmid pRL1JI, encodes a secreted protein. J Bacteriol 171:6764–6770

    PubMed  Google Scholar 

  • D’Haeze W, Gao M-S, De Rycke R, Van Montagu M, Engler G, Holsters M (1998) Roles for Azorhizobial Nod factors and surface polysaccharides in intercellular invasion and nodule penetration, respectively. Mol Plant Microbe Interact 11:999–1008

    CAS  Google Scholar 

  • Downie JA (1998) Functions of rhizobial nodulation genes. In: Spaink HP, Kondorosi A, Hooykaas JP (eds) The Rhizobiaceae. Kluwer, Dordrecht, pp 387–402

    Google Scholar 

  • Dörr J, Hurek T, Reinhold-Hurek B (1998) Type IV pili are involved in plant-microbe and fungus-microbe interactions. Mol Microbiol 30:7–17

    Article  PubMed  Google Scholar 

  • Downie JA, Surin BP (1990) Either of two nod gene loci can complement the nodulation defect of a nod deletionmutant of Rhizobium leguminosarum bv viciae. MolGen Genet 222:81–86

    CAS  Google Scholar 

  • Economou A, Hamilton WD, Johnston AW, Downie JA (1990) The Rhizobium nodulation gene nodO encodes a Ca2+ binding protein that is exported without N-terminal cleavage and is homologous to haemolysin and related proteins. EMBO J 9:349–354

    PubMed  CAS  Google Scholar 

  • Economou A, Davies AE, Johannes E, Downie JA (1994) The Rhizobium leguminosarum biovar vicia nodO gene can enable a nodE mutant of Rhizobium leguminosarum biover trifolii to nodulate vetch. Microbiology 140:2341–2347

    CAS  Google Scholar 

  • Feldman MF, Cornelis GR (2003) Themultitalented type III chaperones: all you can do with 15 kDa. FEMS Microbiol Lett 219:151–158

    Article  PubMed  CAS  Google Scholar 

  • Finnie C, Zorreguieta A, Hartley NM, Downie JA (1998) Characterization of Rhizobium leguminosarum exopolysaccharide glycanases that are secreted via a type I exporter and have a novel heptapeptide repeat motif. J Bacteriol 180:1691–1699

    PubMed  CAS  Google Scholar 

  • Fisher RF, Long SR (1992) Rhizobium-plant signal exchange. Nature 357:655–660

    Article  PubMed  CAS  Google Scholar 

  • Franssen HJ, Vijn I, Yang WC, Bisseling T (1992) Developmental aspects of the hizobiumlegume symbiosis. Plant Mol Biol 19:89–107

    Article  PubMed  CAS  Google Scholar 

  • Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394–401

    Article  PubMed  CAS  Google Scholar 

  • Galibert F, Finan TM, Long SR, Puhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P, Bothe G, Boutry M, Bowser L, Buhrmester J, Cadieu E, Capela D, Chain P, Cowie A, Davis RW, Dreano S, Federspiel NA, Fisher RF, Gloux S, Godrie T, Goffeau A, Golding B, Gouzy J, Gurjal M, Hernandez-Lucas I, Hong A, Huizar L, Hyman RW, Jones T, Kahn D, Kahn ML, Kalman S, Keating DH, Kiss E, Komp C, Lelaure V, Masuy D, Palm C, Peck MC, Pohl TM, Portetelle D, Purnelle B, Ramsperger U, Surzycki R, Thebault P, Vandenbol M, Vorholter FJ, Weidner S, Wells DH, Wong K, Yeh KC, Batut J (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672

    Article  PubMed  CAS  Google Scholar 

  • Geelen D, Goethals K, Van Montagu M, Holsters M (1995) The nodD locus from Azorhizobium caulinodans is flanked by two repetitive elements. Gene 164:107–111

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez V, Bustos P, Ramirez-Romero MA, Medrano-Soto A, Salgado H, Hernandez-Gonzalez I, Hernandez-Celis JC, Quintero V, Moreno-Hagelsieb G, Girard L, Rodriguez O, Flores M, Cevallos MA, Collado-Vides J, Romero D, Davila G (2003) The mosaic structure of the symbiotic plasmid of Rhizobium etil CFN42 and its relation to other symbiotic genome compartments. Genome Biol 4:R36

    Article  PubMed  Google Scholar 

  • Göttfert M, Röthlisberger S, Kündig C, Beck C, Marty R, Hennecke H (2001) Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. J Bacteriol 183:1405–1412

    Article  PubMed  Google Scholar 

  • Hanin M, Jabbouri S, Broughton WJ, Fellay R, Quesada-Vincens D (1999) Molecular aspects of host-specific nodulation. In: Stacey G, Keen NT (eds) Plant-microbe interaction. American Phytopathological Society, St Paul, MN, pp 1–37

    Google Scholar 

  • He SY (1998) Type III protein secretion systems in bacterial pathogenic bacteria. Annu Rev Phytopathol 36:363–392

    Article  PubMed  CAS  Google Scholar 

  • He SY, Jin Q (2003) The Hrp pilus: learning from flagella. Curr Opin Microbiol 6:15–19

    Article  PubMed  CAS  Google Scholar 

  • Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62:379–433

    PubMed  CAS  Google Scholar 

  • Huguet E, Bonas U (1997) hrpF of Xanthomonas campestris pv. vesicatoria encodes an 87-kDa protein with homology to NoIX of Rhizobium fredii. Mol Plant Microbe Interact 10:488–498

    PubMed  CAS  Google Scholar 

  • Jabbouri S, Fellay R, Talmont F, Kamalaprija P, Burger U, Relić B, Prome JC, Broughton WJ (1995) Involvement of nodS in N-methylation and nodU in 6-O-carbamoylation of Rhizobium sp. NGR234 Nod factors. J Biol Chem 270:22968–22973

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:331–338

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K, Kohara M, Matsumoto M, Shimpo S, Tsuruoka H, Wada T, Yamada M, Tabata S (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197

    Article  PubMed  Google Scholar 

  • Kobayashi H, Naciri-Graven Y, Broughton W, Perret X (2004) Flavonoids induce temporal shifts in gene expression of nod-box controlled loci in Rhizobium sp. NGR234. Mol Microbiol 51:335–347

    Article  PubMed  CAS  Google Scholar 

  • Krause A, Doerfel A, Göttfert M (2002) Mutational and transcriptional analysis of the type III secretion system of Bradyrhizobium japonicum. Mol Plant Microbe Interact 15:1228–1235

    PubMed  CAS  Google Scholar 

  • Krishnan HB (2002) NolX of Sinorhizobium fredii USDA257, a type III-secreted protein involved in host range determination, Is localized in the infection threads of cowpea (Vigna unguiculata [L.] Walp) and soybean (Glycinemax [L.] Merr.) nodules. J Bacteriol 184:831–839

    PubMed  CAS  Google Scholar 

  • Krishnan HB, Pueppke SG (1993) Flavonoid inducers of nodulation genes stimulate hizobium fredii USDA257 to export proteins into the environment. Mol Plant Microbe Interact 6:107–113

    PubMed  CAS  Google Scholar 

  • Krishnan HB, Kuo C-I, Pueppke SG (1995) Elaboration of flavonoid-induced proteins by the nitrogen-fixing soybean symbiont Rhizobiumfriedii is regulated by both nodD1 and nodD2, and is dependent on the cultivar-specificity locus, nolXWBTUV. Microbiology 141:2245–2251

    Article  CAS  Google Scholar 

  • Krishnan HB, Lorio J, Kim WS, Jiang G, Kim KY, DeBoer M, Pueppke SG (2003) Extracellular proteins involved in soybean cultivar-specific nodulation are associated with pilus-like surface appendages and exported by a type III protein secretion systemin Sinorhizobium fredii USDA257. Mol Plant Microbe Interact 16:617–625

    PubMed  CAS  Google Scholar 

  • Marie C, Broughton WJ, Deakin WJ (2001) Rhizobium type III secretion systems: legume charmers or alarmers? Curr Opin Plant Biol 4:336–342

    Article  PubMed  CAS  Google Scholar 

  • Marie C, Deakin WJ, Viprey V, Kopcinska J, Golinowski W, Krishnan HB, Perret X, Broughton WJ (2003) Characterization of Nops, nodulation outer proteins, secreted via the type III secretion system of NGR234. Mol Plant Microbe Interact 16:743–751

    PubMed  CAS  Google Scholar 

  • Moreira LM, Becker JD, Puhler A, Becker A (2000) The Sinorhizobium meliloti ExpE1 protein secreted by a type I secretion system involving ExpD1 and ExpD2 is required for biosynthesis or secretion of the exopolysaccharide galactoglucan. Microbiology 146:2237–2248

    PubMed  CAS  Google Scholar 

  • Peabody CR, Chung YJ, Yen MR, Vidal-Ingigliardi D, Pugsley AP, Saier MH (2003) Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051–3072

    Article  PubMed  CAS  Google Scholar 

  • Perret X, Freiberg C, Rosenthal A, Broughton WJ, Fellay R (1999) High-resolution transcriptional analysis of the symbiotic plasmid of Rhizobium sp. NGR234. Mol Microbiol 32:415–425

    Article  PubMed  CAS  Google Scholar 

  • Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201

    Article  PubMed  CAS  Google Scholar 

  • Pueppke SG, Broughton WJ (1999) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant Microbe Interact 12:293–318

    PubMed  CAS  Google Scholar 

  • Pugsley AP (1993) The complete general secretory pathway in Gramnegative bacteria. Microbiol Rev 57:50–108

    PubMed  CAS  Google Scholar 

  • Relić B, Talmont F, Kopcinska J, Golinowski W, Prome JC, Broughton WJ. (1993) Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptilium atropurpureum. Mol Plant Microbe Interact 6:764–774

    PubMed  Google Scholar 

  • Relić B, Perret X, Estrada-Garcia MT, Kopcinska J, Golinowski W, Krishnan HB, Pueppke SG, Broughton WJ (1994) Nod factors of Rhizobium are a key to the legume door. Mol Microbiol 13:171–178

    Article  PubMed  Google Scholar 

  • Rossier O, Van den Ackerveken G, Bonas U (2000) HrpB2 and HrpF from Xanthomonas are type III-secreted proteins and essential for pathogenicity and recognition by the host plant. Mol Microbiol 38:828–838

    Article  PubMed  CAS  Google Scholar 

  • Sandkvist M (2001) Biology of type II secretion. Mol Microbiol 40:271–283

    Article  PubMed  CAS  Google Scholar 

  • Spaink HP, Sheeley DM, van Brussel AA, Glushka J, York WS, Tak T, Geiger O, Kennedy EP, Reinhold VN, Lugtenberg BJ (1991) A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium Nature 354:125–130

    Article  PubMed  CAS  Google Scholar 

  • Stacey G, So JS, Roth LE, Bhagya Lakshmi SK, Carlson RW (1991) A lipopolysaccharide mutant of Bradyrhizobium japonicum that uncouples plant from bacterial differentiation. Mol Plant Microbe Interact 4:332–340

    PubMed  CAS  Google Scholar 

  • Streit WR, Schmitz RA, Perret X, Staehelin C, Deakin WJ, Raasch C, Liesegang H, Broughton WJ (2004) An evolutionary hot spot: the pNGR234b replicon of Rhizobium sp. Strain NGR234. J Bacteriol 186:535–542

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JT, Trzebiatowski JR, Cruickshank RW, Gouzy J, Brown ST, Elliot RM, Fleetwood DJ, McCallum NG, Rossbach U, Stuart GS, Weaver JE, Webby RJ, de Bruijn FJ, Ronson cw (2002) Comparative sequence analysis of the symbiosis island of Mesorhizobium loti StrainR7A. J Bacteriol 184:3086–3095

    Article  PubMed  CAS  Google Scholar 

  • Sutton JM, Lea EJ, Downie JA (1994) The nodulation-signalling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc Natl Acad Sci USA 91:9990–9994

    Article  PubMed  CAS  Google Scholar 

  • Sutton JM, Peart J, Dean G, Downie JA (1996) Analysis of the C-terminal secretion signal of the Rhizobium leguminosarum nodulation protein NodO; a potential system for the secretion of heterologous proteins during nodule invasion. Mol Plant Microbe Interact 9:671–680

    PubMed  CAS  Google Scholar 

  • Thanassi DG, Hultgren SJ (2000) Multiple pathways allow protein secretion across the bacterial outer membrane. Curr Opin Cell Biol 12:420–430

    Article  PubMed  CAS  Google Scholar 

  • Trinick MJ (1980) Relationships amongst the fast-growing rhizobia of Lablab purpureus, Leucaena leucocephala, Mimosa spp., Acacia farnesiana and Sesbania grandiflora and their affinities with other rhizobial groups. J Appl Bacteriol 49:39–53

    Google Scholar 

  • Van Rhijn P, Luyten E, Vlassak K, Vanderleyden J (1996) Isolation and characterization of a pSym locus of Rhizobium sp. BR816 that extends nodulation ability of narrow host range Phaseolus vulgaris symbionts to Leucaena leucocephala Mol Plant Microbe Interact 9:74–77

    PubMed  Google Scholar 

  • Van Spronsen PC, Bakhuizen R, van Brussel AA, Kijne JW (1994) Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process. Eur J Cell Biol 64:88–94

    PubMed  Google Scholar 

  • Viprey V, DelGreco A, Golinowski W, Broughton WJ, Perret X (1998) Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol Microbiol 28:1381–1389

    Article  PubMed  CAS  Google Scholar 

  • Vlassak KM, de Wilde P, Snoeck C, Luyten E, van Rhijn P, Vanderleyden J (1998) The Rhizobium sp. BR816 nodD3 gene is regulated by a transcriptional regulator of the AraC/XylS family. Mol Gen Genet 258:558–561

    Article  PubMed  CAS  Google Scholar 

  • Walker SA, Downie JA (2000) Entry of Rhizobium leguminosarum bv. viciae into root hairs requires minimal Nod factor specificity, but subsequent infection thread growth requires nodO or nodE Mol Plant Microbe Interact 13:754–762

    PubMed  CAS  Google Scholar 

  • Winans SC, Burns DL, Christie PJ (1996) Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol 4:64–68

    Article  PubMed  CAS  Google Scholar 

  • Wolfgang M, van Putten JP, Hayes SF, Dorward D, Koomey M (2000) Components and dynamics of fibres formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J 19:6408–6418

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Biologie Moléculaire des Plantes Supérieures, Sciences III, Université de Genève, 30 Quai Ernest-Ansermet, 1211, Genève 4, Switzerland

    Maged M. Saad, William J. Broughton & William J. Deakin

Authors
  1. Maged M. Saad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. William J. Broughton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William J. Deakin
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Institute of Microbiology, Technical University of Braunschweig, Spielmannstraße 7, 38106, Braunschweig, Germany

    Barbara J. E. Schulz

  2. Augustastraße 32, 02826, Görlitz, Germany

    Christine J. C. Boyle

  3. Department of Environmental Sciences Institute of Integrative Biology Forest Pathology and Dendrology, Swiss Federal Institute of Technology, 8092, Zürich, Switzerland

    Thomas N. Sieber

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Saad, M.M., Broughton, W.J., Deakin, W.J. (2006). Role of Proteins Secreted by Rhizobia in Symbiotic Interactions with Leguminous Roots. In: Schulz, B.J.E., Boyle, C.J.C., Sieber, T.N. (eds) Microbial Root Endophytes. Soil Biology, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-33526-9_5

Download citation

Publish with us

Policies and ethics

Search

Navigation