Skip to main content
Book cover

Root Hairs pp 241–265Cite as

Nod-Factors in Symbiotic Development of Root Hairs

  • Chapter

Abstract

Generally, root hairs emerge at the apical end of some epidermal cells, and elongate by polar growth of the tip (Cormack 1962; see Chapters 1 to 3 this volume). Young, elongating root hairs are extensively colonized by soil-borne micro-organisms. Intimate associations between dissimilar organisms are common, especially in nutrient poor environments. Prevalent amongst these associations are nitrogen-fixing symbioses in which photosynthetic organisms provide carbohydrates in exchange for organic nitrogen exported by diazotrophs. Soil bacteria of the genera Azorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium (collectively called rhizobia) enter the roots (and occasionally adventitious-roots on the stems) of legumes (family Leguminosae), and induce the formation of highly specialised organs, called nodules. Rhizobia present in the root nodules convert to an endo-symbiotic form, the bacteroids, in which dinitrogen is reduced to ammonia. Bacteroids within nodules contribute a disproportionately large portion of fixed nitrogen to the global pool.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   109.99
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

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aguilar J, Ashby A, Richards J, Loake G, Watson M, Shaw C (1988) Chemotaxis of Rhizobium leguminosarum biovar phaseoli towards flavonoids inducers of the symbiotic nodulation genes. J Gen Microbiol 134: 2741–2746

    Google Scholar 

  • Albrecht C, Guerts R, Bisseling T (1999) Legume nodulation and mycorrhizae formation: two extremes in host specificity meet. EMBO J 18: 281–288

    PubMed  CAS  Google Scholar 

  • Allen E, Allen O, Newman A (1953) Pseudonodulation of leguminous plants induced by 2bromo-3,5-dichlorobenzoic acid. Am J Bot 40: 429–435

    CAS  Google Scholar 

  • Allen NS, Bennett MS, Cox D, N, Shipley A, Ehrhardt DW, Long SR (1994) Effects of Nod-factors on alfalfa root hair Ca++ and H+ currents and on cytoskeletal behavior. In: Daniels M (Ed) Advances in molecular genetics of plant-microbe interactions. Kluwer Academic Publishers, Dordecht, pp 107–113

    Google Scholar 

  • Allison L, Kiss G, Bauer P, Poiret M, Pierre M, Savouré A, Kondorosi E, Kondorosi A (1993) Identification of two alfalfa early nodulin genes with homology to members of the pea Enod12 gene family. Plant Mol Biol 21: 375–380

    PubMed  CAS  Google Scholar 

  • Ardourel M, Demont N, Debellé F, Maillet F, de Billy F, Promé J-C, Dénarié J, Truchet G (1994) Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6: 1357–1374

    Google Scholar 

  • Arsenijevié -Maksimovié I, Broughton W, Krause A (1997) Rhizobia modulate root-hair specific expression of extensin genes. Mol Plant-Micr Inter 10: 95–101

    Google Scholar 

  • Barbour WM, Hattermann DR, Stacey G (1991) Chemotaxis of Bradyrhizobium to soybean exudates. Appl Environ Microbiol 57: 2635–2639.

    PubMed  CAS  Google Scholar 

  • Baskin T, Wilson J, Cork A, Williamson R (1994) Morphology and microtubule organization in Arabidopsis roots exposed to oryzalin or taxol. Plant Cell Physiol 35: 935–942

    PubMed  CAS  Google Scholar 

  • Biswas S, Dalai B, Sen M, Biswas B (1995) Receptor for myo-inositol trisphosphate from the microsomal fraction of Vigna radiata. Biochem J 306: 631–636

    PubMed  CAS  Google Scholar 

  • Blumwald E, Aharon GS, Lam BC-H (1998) Early signal transduction pathways in plant-pathogen interactions. Trends Plant Sci 3: 342–346

    Google Scholar 

  • Bonnett H, Newcomb E (1966) Coated vesicles and other cytoplasmic components of root hairs of radish. Protoplasma 62: 59–75

    Google Scholar 

  • Bono J-J, Riond J, Nicolaou K, Bockovich NJ, Estevez VA, Cullimore JV, Ranjeva R (1995) Characterization of a binding site for chemically synthesized lipooligosaccharidic NodRm factors in particulate fractions prepared from roots. Plant J 7: 253–260

    PubMed  CAS  Google Scholar 

  • Briskin DP, Leonard RT, Hodges TK (1987) Isolation of the plasma membrane: Membrane markers and general principles. Meth Enz 148: 542–575

    Google Scholar 

  • Broughton W (1978) Control of specificity in legume-Rhizobium associations. J Appl Bact 45: 165–194

    Google Scholar 

  • Cardenas L, Vidali L, Dominguez J, Peréz H, Sanchez F, Hepler P, Quinto C (1998) Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals. Plant Physiol 116: 871–877

    CAS  Google Scholar 

  • Cohn J, Day BR, Stacey G (1998) Legume nodule organogenesis. Trends Plant Sci 3: 105110

    Google Scholar 

  • Cormack R (1962) Development of root hairs in angiosperms. II. Bot Rev 28: 446–464

    CAS  Google Scholar 

  • Coté GG, Crain RC (1993) Biochemistry of phosphoinositides. Annu Rev Plant Physiol Plant Mol Biol 44: 333–356

    Google Scholar 

  • Csanadi G, Szécsi J, Kaló P, Kiss P, Endre G, Kondorosi A, Kondorosi E, Kiss G (1994) ENOD12, an early nodulin gene, is not required for nodule formation and efficient nitrogen fixation in alfalfa. Plant Cell 6: 201–213

    Google Scholar 

  • Dart P (1977) Infection and development of leguminous nodules. In Hardy R, Silver W (Eds) A treatise on dinitrogen fixation, Sect. III. Cambridge University Press, London, pp 367–472

    Google Scholar 

  • Ruijter N, Rook M, Bisseling T, Emons A (1998) Lipochito-oligosaccharides re-initiate root. hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J 13: 341–350

    Google Scholar 

  • Dénarié J, Debellé F, Promé J-C (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503–535

    Google Scholar 

  • D’Haeze W, Gao M-S, de Rycke R, van Monatagu M, Engler G, Holsters M (1998) Roles for azorhizobial Nod-factors and surface polysaccharides in intercellular invasion and nodule penetration, respectively. Mol Plant-Micr Inter 11: 999–1008

    Google Scholar 

  • Dharmatilake A, Bauer W (1992) Chemotaxis of Rhizobium meliloti towards nodulation gene-inducing compounds from alfalfa roots. Appl Environ Microbiol 58: 1153–1158

    PubMed  CAS  Google Scholar 

  • Djordjevic MA, Gabriel DW, Rolfe BG (1987) Rhizobium - the refined parasite of legumes. Annu Rev Phytopath 25: 145–168

    Google Scholar 

  • Dobert R, Rood S, Blevins D (1992) Gibberellins and the legume-Rhizobium symbiosis. Plant Physiol 98: 221–224

    PubMed  CAS  Google Scholar 

  • DrObak BK, Watkins PAC, Valenta R, Dove SK, Lloyd CW, Staiger CJ (1994) Inhibition of plant plasma membrane phosphoinositide phospholipase C by the actin-binding protein, profilin. Plant J 6: 389–400

    Google Scholar 

  • Ehrhardt DW, Atkinson EM, Long SR (1992) Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod-factors. Science 256: 998–1000

    PubMed  CAS  Google Scholar 

  • Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85: 673–681

    PubMed  CAS  Google Scholar 

  • Emons A (1987) The cytoskeleton and secretory vesicles in root hairs of Equisetum and Linnobium and cytoplasmic streaming in root hairs of Equisetum. Ann Bot 60: 625–632

    Google Scholar 

  • Estabrook EM, Sengupta-Gopalan C (1991) Differential expression of phenylalanine ammonia-lyase and chalcone synthase during soybean nodule development. Plant Cell 3: 299–308

    PubMed  CAS  Google Scholar 

  • Farmer EE, Moloshok TD, Saxton MI, Ryan CA (1991) Oligosaccharide signalling in Plants. Specificity of oligouronide-enhanced plasma membrane phosphorylation. J Biol Chem 266: 3140–3145

    Google Scholar 

  • Felle HH, Kondorosi E, Kondorosi A, Schultze M (1995) Nod signal-induced plasma membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipochitooligosaccharide. Plant J 7: 939–947

    CAS  Google Scholar 

  • Felle HH, Kondorosi E, Kondorosi A, Schultze M (1996) Rapid alkalinization in alfalfa root hairs in response to rhizobial lipochitooligosaccharide signals. Plant J 10: 295–301

    CAS  Google Scholar 

  • Felle HH, Kondorosi E, Kondorosi A, Schultze M (1998) The role of ion fluxes in Nod-factor signalling in Medicago sativa. Plant J 13: 455–463

    CAS  Google Scholar 

  • Ruhr R (1998) Ethylene perception: from two-component signal tranducers to gene induction. Trends Plant Sci 3: 141–146

    Google Scholar 

  • Galway M, Heckman J, Schiefelbein J (1997) Growth and ultrastructure of Arabidopsis root hairs: the rhd3 mutation alters vacuole enlargement and tip growth. Planta 201: 209–218

    PubMed  CAS  Google Scholar 

  • Gehring CA, Irving HR, Kabbara AA, Parish RW, Boukli NM, Broughton WJ (1997) Rapid, plateau-like increases in intracellular free calcium are associated with Nodfactor-induced root hair deformation. Mol Plant-Micr Inter 10: 791–802

    CAS  Google Scholar 

  • Gressent F, Drouillard GF, Mantegazza S, Samain E, Geremia RA, Niebel A, Driguez H, Ranjeva R, Cullimore J, Bono JJ (1999) Ligand specificity of a high-affinity binding site for lipo-chitooligosaccharide Nod-factors in Medicago suspension cultures Proc Natl Acad Sci 96: 4704–4709.

    CAS  Google Scholar 

  • Halbrock K, Scheel D (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 40: 347–369

    Google Scholar 

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

    Google Scholar 

  • Hartwig U, Maxwell C, Joseph C, Philips D (1990) Effects of alfalfa nod gene-inducing flavonoids on nodABC transcription in Rhizobium meliloti strains containing different nodD genes. J Bacteriol 172: 2769–2773

    PubMed  CAS  Google Scholar 

  • Hartwig U, Philips D (1991) Release and modification of nod-gene-inducing flavonoids from alfalfa seeds. Plant Physiol 95: 804–807

    PubMed  CAS  Google Scholar 

  • Heidstra R, Guerts R, Franssen H, Spaink H, van Kammen A, Bisseling T (1994) Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol 105: 787–797

    PubMed  CAS  Google Scholar 

  • Heidstra R, Yang W, Yalcin Y, Peck S, Emons A, van Kammen A, Bisseling T (1997) Ethylene provides positional information on cortical cell division but is not involved in Nod-factor-induced root hair tip growth in Rhizobium-legume interaction. Development 124: 1781–1787

    PubMed  CAS  Google Scholar 

  • Helal H, Sauerbeck D (1989) Carbon turnover in the rhizosphere. Z Pflanzenernahr Bodenk 152: 211–216

    CAS  Google Scholar 

  • Hirsch, AM (1992) Tansley Review No. 40. Developmental biology of legume nodulation. New Phytol 122: 211–237

    Google Scholar 

  • Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors Proc Natl Acad Sci 86: 1244–1248.

    CAS  Google Scholar 

  • Hirsch A, Fang Y (1994) Plant hormones and nodulation: what’s the connection? Plant Mol Bio1:5–9 15. Nod-Factors in Symbiotic Development of Root Hairs 261

    Google Scholar 

  • Hirsch AM, Fang Y, Asad S, Kapulink Y (1997) The role of phytohormones in plant-microbe symbioses. Plant Soil 194: 171–184

    CAS  Google Scholar 

  • Hirsch AM, Kapulnik Y (1998) Signal transduction pathways in mycorrhizal associations: Comparisons with the Rhizobium-legume symbiosis. Fungal Genet. Biol. 23: 205–212

    Google Scholar 

  • Hiscock S, Kues U, Dickinson H (1996) Molecular mechanisms of self-incompatibility in flowering plants and fungi - different means to the same end. Trends Cell Biol 6: 421428

    Google Scholar 

  • Horvath B, Heidstra R, Lados M, Moerman M, Spaink H, Promé J-C, van Kammen A, Bisseling T (1993) Lipo-chitoligosaccharides of Rhizobium induce infection-related early nodulin gene expression in pea root hairs. Plant J 4: 723–764

    Google Scholar 

  • Hungria M, Johnston A, Philips D (1992) Effects of flavonoids released naturally from bean (Phaseolus vulgaris) on nodD-regulated gene transcription in Rhizobium leguminosarum by. viciae. Mol Plant-Micr Inter 5: 199–203

    CAS  Google Scholar 

  • Hungria M, Joseph C, Philips D (1991a) Anthocyanidins and flavonols: major nod gene inducers from seeds of a black-seeded common bean (Phaseolus vulagaris L). Plant Physiol 97: 751–758

    PubMed  CAS  Google Scholar 

  • Hungria M, Joseph C, Philips D (1991b) Rhizobium nod gene inducers exuded naturally from roots of common bean (Phaseolus vulgaris L). Plant Physiol 97: 759–764

    Google Scholar 

  • Jacobs M, Rubery PH (1988) Naturally occurring auxin transport regulators. Science 241: 346–349

    PubMed  CAS  Google Scholar 

  • Junghans H, Dalkin K, Dixon RA (1993) Stress responses in alfalfa (Medicago sativa L.). 15. Characterizations and expression patterns of members of a subset of the chalcone synthase multigene family. Plant Mol Biol 22: 239–253

    Google Scholar 

  • Kape R, Parniske M, Brandt S, Werner D (1992) Isoliquiritigenin, a strong nod gene-and glyceollin resistance-inducing flavonoid from soybean root exudate. Appl Environ Microbiol 58: 1705–1710

    PubMed  CAS  Google Scholar 

  • Kellis J, Vickery L (1984) Inhibition of human estrogen synthetase (aromatase) by flavones. Science 225: 1032–1034

    PubMed  CAS  Google Scholar 

  • Kijne J (1992) The Rhizobium infection process. In Stacey G, Burris R Evans H (Eds) Biological nitrogen fixation. Chapman and Hall, New York, pp 349–398

    Google Scholar 

  • Kosslak R, Bookland R, Barkei J, Paaren H, Appelbaum E (1987) Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc Natl Acad Sci USA 84: 7428–7432

    PubMed  CAS  Google Scholar 

  • Krause A, Broughton WJ (1992) Proteins associated with root-hair deformation and nodule initiation in Vigna unguiculata. Mol Plant-Micr Inter 5: 96–103

    CAS  Google Scholar 

  • Krause A, Lan VT, Broughton WJ (1997) Induction of chalcone synthase expression by rhizobia and Nod-factors in root hairs and roots. Mol Plant-Micr Inter 10: 388–393

    CAS  Google Scholar 

  • Krause A, Sigrist CJ, Dehning I, Sommer H, Broughton WJ (1994) Accumùlation of transcripts encoding a lipid transfer-like protein during deformation of nodulationcompetent Vigna unguiculata root hairs. Mol Plant-Micr Inter 7: 411–418

    CAS  Google Scholar 

  • Kurkdjian AC (1995) Role of the differentiation of root epidermal cells in Nod-factor (from Rhizobium meliloti)-induced root-hair depolarisation of Medicago sativa. Plant Physiol 107: 783–790

    PubMed  CAS  Google Scholar 

  • Lawson CGR, Djordjevic MA, Weinman JJ, Rolfe BG (1994) Rhizobium inoculation and physical wounding result in the rapid induction of the same chalcone synthase copy in Trifolium subterraneum. Mol Plant-Microbe Interact 7: 498–507

    Google Scholar 

  • Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, Dénarié J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781–784

    PubMed  CAS  Google Scholar 

  • Lin Y, Wang Y, Zhu J-k, Yang Z (1996) Localization of a Rho GTPase implies a role in tip growth and movement of the generative cell in pollen tubes. Plant Cell 8: 293–303

    PubMed  CAS  Google Scholar 

  • Long SR (1996) Rhizobium symbiosis: Nod-factors in perspective. Plant Cell 8:1885–1898 Ma H (1994) GTP-binding proteins in plants: new members of an old family. Plant Mol Biol 26:1611–1636

    Google Scholar 

  • Mathesius U, Bayliss C, Weinman JJ, Schlaman HRM, Spaink HP, Rolfe BG, McCully ME, Djordjevic MA (1998a) Flavonoids synthesized in cortical cells during nodule initiation are early developmental markers in white clover Mol Plant-Microbe Interact 11: 1223–1232

    CAS  Google Scholar 

  • Mathesius U, Schlaman H, Spaink H, Sautter C, Rolfe B, Djordjevic M (1998b) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14: 23–34

    PubMed  CAS  Google Scholar 

  • Maxwell C, Philips D (1990) Concurrent synthesis and release of nod-gene-inducing flavonoids from alfalfa roots. Plant Physiol 93: 1552–1558

    PubMed  CAS  Google Scholar 

  • McKhann HI, Hirsch AM (1994) Isolation of chalcone synthase and chalcone isomerase cDNAs from alfalfa (Medicago sativa L.): highest transcript levels occur in young roots and root tips. Plant Mol Biol 24: 767–777

    PubMed  CAS  Google Scholar 

  • McKhann H, Paiva N, Dixon R, Hirsch A (1997) Chalcone synthase transcripts are detected in alfalfa root hairs following inoculation with wild-type Rhizobium meliloti. Mol PlantMicr Inter 10: 50–58

    CAS  Google Scholar 

  • McKhann HI, Paiva NL, Dixon RA, Hirsch AM (1998) Expression of genes for enzymes of the flavonoid biosynthetic pathway in the early stages of the Rhizobium-legume symbiosis. In Flavonoids in the living system. J. Manthey and B. Buslig (Eds), Plenum Press, New York. pp. 45–54.

    Google Scholar 

  • Mergaert P, van Montagu M, Promé J-C, Holsters M (1993) Three unusual modifications, a D-arabinosyl, an N-methyl, and a carbamoyl group, are present on the Nod-factors of Azorhizobium caulinodans strain ORS571. Proc Natl Acad Sci USA 90: 1551–1555

    PubMed  CAS  Google Scholar 

  • Miller DD, de Ruijter NC, Bisseling T, Emons AMC (1999) The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J 17: 141–154

    CAS  Google Scholar 

  • Miller DD, de Ruijter NC, Emons AMC (1997) From signal to form: aspects of the cytoskeleton-plasma membrane-cell wall continuum in root hair tips. J Exp Bot 48: 1881–1896

    CAS  Google Scholar 

  • Minami E, Kouchi H, Carlson R, Cohn J, Kolli V, Day R, Ogawa T, Stacey G (1996a) Cooperative action of lipo-chitin nodulation signals on the induction of the early nodulin, ENOD2, in soybean roots. Mol Plant-Micr Inter 9: 574–583

    CAS  Google Scholar 

  • Minami E, Kouchi H, Cohn J, Ogawa T, Stacey G (1996b) Expression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules. Plant J 10: 23–32

    PubMed  CAS  Google Scholar 

  • Niebel A, Bono J, Ranjeva R, Cullimore J (1997) Identification of a high affinity binding site for lipo-oligosaccharidic NodRm factors in the microsomal fraction of Medicago cell suspension cultures. Mol Plant-Micr Inter 10: 132–134

    CAS  Google Scholar 

  • Penmetsa R, Cook D (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275: 527–530

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pichon M, Journet E-P, Dedieu A, de Billy F, Truchet G, Barker D (1992) Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell 4: 1199–1211

    Google Scholar 

  • Philip-Hollingsworth S, Da77o FB, Hollingsworth RI (1997) Structural requirements of Rhizobium chitooligosaccharides for uptake and bioactivity in legume roots as revealed by synthetic analogs and fluorescent probes. J Lipid Res 38: 1229–1241

    PubMed  CAS  Google Scholar 

  • Pingret J-L, Joumet E-P, Barker DG (1998) Rhizobium Nod-factor signaling: Evidence for a G protein-mediated transduction mechanism. Plant Cell 10: 659–671

    Google Scholar 

  • Price N, Relic B, Talmont F, Lewin A, Promé D, Pueppke S, Maillet F, Dénarié J, Promé J-C, Broughton W (1992) Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated nodulation signals that are O-acetylated or sulphated. Mol Microbiol 6: 3575–3584

    PubMed  CAS  Google Scholar 

  • Rao J, Cooper J (1994) Rhizobia catabolize nod gene inducing flavonoids via C-ring fission mechanisms. J Bacteriol 176: 5409–5413

    PubMed  CAS  Google Scholar 

  • Rao J, Cooper J (1995) Soybean nodulating rhizobia modify nod gene inducers daidzein and genistein to yield aromatic products that can influence gene inducing activity. Mol Plant-Micr Inter 8: 855–862

    CAS  Google Scholar 

  • Recourt K, Schripsema J, Kijne J, van Brussel A, Lugtenberg B (1991) Inoculation of Viciae sativa subsp. nigra roots with Rhizobium leguminosarum by. viciae results in release of nod gene activating flavanones and chalcones. Plant Mol Biol 16: 841–852

    PubMed  CAS  Google Scholar 

  • Recourt K, Verkerke M, Schripsema J, van Brussel A, Lugtenberg B, Kijne J (1992) Major flavonoids in uninoculated and inoculated roots of Viciae sativa subsp. nigra are four conjugates of the nodulation gene inhibitor kaempferol. Plant Mol Biol 18: 505–513

    PubMed  CAS  Google Scholar 

  • Redmond J, Batley M, Djordjevic M, Innes R, Kuempel P, Rolfe B (1986) Flavones induce expression of nodulation genes in Rhizobium. Nature 323: 632–635

    CAS  Google Scholar 

  • Relic 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

    PubMed  CAS  Google Scholar 

  • Relic B, Talmont F, Kopcinska J, Golinowski W, Promé J-C, Broughton WJ (1993) Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptilium atropurpureum. Mol Plant-Micr Inter 6: 764–774

    CAS  Google Scholar 

  • Ridge R (1988) Freeze substitution improves the ultrastructural preservation of legume root hairs. Bot Mag Tokyo 101: 427–441

    Google Scholar 

  • Ridge RW (1992) A model of legume root hair growth and Rhizobium infection. Symbiosis 14: 359–373

    Google Scholar 

  • Sanjuan J, Carlson R, Spaink H, Bhat U, Barbour W, Glushka J, Stacey G (1992) A 2–0methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proc Natl Acad Sci USA 89: 8789–8793

    PubMed  CAS  Google Scholar 

  • Scheres B, McKhan H, Zalensky A, Löbler M, Bisseling T, Hirsch A (1992) The PsENOD12 gene is expressed at two different sites in Afghanistan pea pseudonodules induced by auxin transport inhibitors. Plant Physiol 100: 1649–1655

    PubMed  CAS  Google Scholar 

  • Scheres B, van de Wiel C, Zalenski A, Horvath B, Spaink H, van Eck H, Zwartkruis F, Wolters A-M, Gloudemans T, van Kammen A, Bisseling T (1990) The Enod12 gene product is involved in the infection process during the pea-Rhizobium interaction. Cell 60: 281–294

    PubMed  CAS  Google Scholar 

  • Schiefelbein J, Somerville C (1990) Genetic control of root hair development in Arabidopsis thaliana. Plant Cell 2: 235–243

    PubMed  CAS  Google Scholar 

  • Schmidt P, Broughton W, Werner D (1994) Nod-factors of Bradyrhizobium japonicum and Rhizobia sp. NGR234 induce flavonoid accumulation in soybean exudate. Mol PlantMicr Inter 7: 384–390

    CAS  Google Scholar 

  • Schultze M, Quiclet-Sire B, Kondorosi E, Virelizier H, Glushka N, Endre G, Géro D, Kondorosi A (1992) Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity. Proc Natl Acad Sci USA 89: 92–196

    Google Scholar 

  • Sherrier D, VandenBosch K (1994) Secretion of cell wall polysaccharides in Vicia root hairs. Plant J 5: 185–195

    CAS  Google Scholar 

  • Singer WD, Brown HA, Sternweis PC (1997) Regulation of eukaryotic phosphatidylinositol-specific phospholipase C and phospholipase D. Annu Rev Biochem 66: 475–509

    PubMed  CAS  Google Scholar 

  • Smertenko A, Jiang C-J, Simmons N, Weeds A, Davies D, Hussey P (1998) Ser6 in the maize actin-depolymerizing factor, ZmADF3, is phosphorylated by a calcium-stimulated protein kinase and is essential for the control of functional activity. Plant J 14: 187–193

    PubMed  CAS  Google Scholar 

  • Smit G, Puvanesarajah V, Carlson RW, Barbour WM, Stacey G (1992) Bradyrhizobium japonicum nodDl can be specifically induced by soybean flavonoids that do not induce the nodYABCSUIJ operon. J biol Chem 267: 310.

    Google Scholar 

  • Spaink H, Sheeley D, van Brussel A, Glushka J, York W, Tak T, Geiger O, Kennedy E, Reinhold V, Lugtenberg B (1991) A novel highly unsaturated fatty acid moiety of lipooligosaccharide signals determines host specificity of Rhizobium. Nature 354: 125–130

    PubMed  CAS  Google Scholar 

  • Staehelin C, Granado J, Müller J, Wiemken A, Mellor B, Felix G, Regenass M, Broughton WJ, and Boller (1994) Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases Proc Natl Acad Sci 91: 2196–2200

    CAS  Google Scholar 

  • Stokkermans J, Peters N (1994) Bradyrhizobium elkanü lipo-oligosaccharide signals induce complete nodule structures on Glycine soja Siebold & Zucc. Planta 193: 413–420

    Google Scholar 

  • Sutherland T, Bassam B, Schuller L, Gresshoff P (1990) Early nodulation signals of the wild type and symbiotic mutants of soybean (Glycine max). Mol Plant-Micr Inter 3: 122–128

    CAS  Google Scholar 

  • Takai T, Sasaki T, Tanaka K, Nakanishi H (1995) Rho as a regulator of the cytoskeleton. Trends Biochem Sci 20: 227–231

    PubMed  CAS  Google Scholar 

  • Tominaga M, Morita K, Sonobe S, Yokota E, Shimmen T (1997) Microtubules regulate the organization of actin filaments at the cortical region in root hair cells of Hydrocharis. Protoplasma 199: 83–92

    CAS  Google Scholar 

  • Truchet G, Roche P, Lerouge P, Vasse J, Camut S, de Billy F, Promé J-C, Dénarié J (1991) Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351: 670–673

    CAS  Google Scholar 

  • Brussel A, Bakhuizen R, van Spronsen P, Spaink H, Tak T, Lugtenberg B, Kijne J (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257: 70–72

    PubMed  Google Scholar 

  • Brussel A, Recourt K, Pees E, Spaink H, Tak T, Wijffelman C, Kijne J, Lugtenberg B (1990) A biovar-specific signal of Rhizobium leguminosarum by. viciae induces increased nodulation gene-inducing activity in root exudate of Vicia sativa subsp. nigra. J Bacteriol 172: 5394–5401

    PubMed  Google Scholar 

  • Workum W, van Brussel A, Tak T, Wijffelman C, Kijne J (1995) Ethylene prevents nodulation of Vicia sativa ssp. nigra by exopolysaccharide-deficient mutants of Rhizobium leguminosarum by. viciae. Mol Plant-Micr Inter 8: 111–119

    Google Scholar 

  • Viel A, Branton D (1996) Spectrin: on the path from structure to function. Curr Opin Cell Biol 8: 49–55

    PubMed  CAS  Google Scholar 

  • Vijn I, Martinez-Abarca F, Yang W, Das Neves L, van Brussel A, van Kammen A, Bisseling T (1995) Early nodulin gene expression during Nod-factor-induced processes in Vicia sativa. Plant J 8: 111–119

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Viprey V, Perret X, Broughton W (2000) Host-plant invasion by Rhizobia. In Hacker J, Olschlager T (Eds) Subcellular biochemistry. Bacterial invasion into eukaryotic cells. Plenum Publishing Corp, London, (in press)

    Google Scholar 

  • Widdell S, Larsson C (1987) Plasma membrane purification. In Senger H (Ed) Blue light responses: Phenomena and occurrence in plants and microorganisms. CRC Press, Boca Raton, Florida, pp 99–107

    Google Scholar 

  • Williams P, de Mallorca S (1982) Abscisic acid and gibberellin-like substances in root and root nodules of Glycine max. Plant Soil 65: 19–26

    CAS  Google Scholar 

  • Wymer C, Wymer S, Cosgrove D, Cyr R (1996) Plant cell growth responds to external forces and the response requires intact microtubules. Plant Physiol 110: 425–430

    PubMed  CAS  Google Scholar 

  • Yoshida S, Uemura M, Niki T, Sakai A, Gusta L (1983) Partition of membrane particles in aqueous two-polymer phase system and its practical use for purification of plasma membranes from plants. Plant Physiol 72: 105–114

    PubMed  CAS  Google Scholar 

  • Zaat S, Schripsema J, Wijffelman C, van Brussel A, Lugtenberg B (1989) Analysis of the major inducers of the Rhizobium nodA promoter from Viciae sativa root exudate and their activity with different nodD genes. Plant Mol Biol 13: 175–188

    PubMed  CAS  Google Scholar 

  • Zhang S, Sheng J, Liu Y, Mehdy M (1993) Fungal elicitor-induced bean proline-rich protein mRNA down-regulation is due to destabilization that is transcription and translation dependent. Plant Cell 5: 1089–1099

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer-Verlag Tokyo

About this chapter

Cite this chapter

Irving, H.R., Boukli, N.M., Kelly, M.N., Broughton, W.J. (2000). Nod-Factors in Symbiotic Development of Root Hairs. In: Ridge, R.W., Emons, A.M.C. (eds) Root Hairs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-68370-4_15

Download citation

  • DOI: https://doi.org/10.1007/978-4-431-68370-4_15

  • Publisher Name: Springer, Tokyo

  • Print ISBN: 978-4-431-68372-8

  • Online ISBN: 978-4-431-68370-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics