Skip to main content
Book cover

Root Hairs pp 267–283Cite as

Rhizobium-Induced Plant Gene Expression in Root Hairs

  • Chapter
  • 267 Accesses

Abstract

Root hairs, seen as an extension and surface enlargement of root epidermal cells, so-called trichoblasts, serve for the uptake of nutrients and provide anchorage into the soil. In addition, the young emerging root hairs are the first cells of legumes with which symbiotic soil bacteria of several genera, collectively called rhizobia, interact (Bhuvaneswari et al. 1980; Broughton and Perret 1999; Turgeon and Bauer 1985). This interaction leads to root nodules, new organs that are formed within the cortex of the root. Here, the bacteria are hosted in order to fix atmospheric nitrogen into ammonia for the benefit of the plant. In return, the host plant pays back by supplying the bacteria with organic nutrients. In several areas soil nitrogen is a limiting factor, and there symbiosis makes leguminous species significantly more competitive than other species.

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

  • Allison LA, Kiss GB, Bauer P, Poiret M, Pierre M, Savoure A, Kondorosi E, Kondorosi A (1993) Identification of two alfalfa early nodulin genes with homology to members of the pea Enodl2 gene family. Plant Mol Bio! 21: 375–80

    Article  CAS  Google Scholar 

  • Arsenijevic Maksimovic I, Broughton WJ, Krause A (1997) Rhizobia modulate root-hairspecific expression of extensin genes. Mol Plant Microbe Interact 10: 95–101

    Article  PubMed  CAS  Google Scholar 

  • Bauer P, Crespi MD, Szecsi J, Allison LA, Schultze M, Ratet P, Kondorosi E, Kondorosi A (1994) Alfalfa Enodl2 genes are differentially regulated during nodule development by Nod-factors and Rhizobium invasion. Plant Physiol 105: 585–92

    Article  PubMed  CAS  Google Scholar 

  • Bauer P, Poirier S, Ratet P, Kondorosi A (1997) MsEnodl2A expression is linked to meristematic activity during development of indeterminate and determinate nodules and roots. Mol Plant Microbe Interact 10: 39–49

    Article  CAS  Google Scholar 

  • Bauer P, Ratet P, Crespi MD, Schultze M, Kondorosi A (1996) Nod-factors and cytokinins induce similar cortical cell division, amyloplast deposition and MsEnodl2A expression patterns in alfalfa roots. Plant J 10: 91–105

    Article  CAS  Google Scholar 

  • Bauer WD (1981) Infection of legumes by rhizobia. Annu Rev Plant Physiol 32: 407–449

    Article  CAS  Google Scholar 

  • Bhuvaneswari TV, Bhagwat AA, Bauer WD (1981) Transient susceptibility of root cells in four common legumes to nodulation by rhizobia. Plant Physiol 68: 1144–1149

    Article  PubMed  CAS  Google Scholar 

  • Bhuvaneswari TV, Mills KK, Crist DK, Evans WR, Bauer WD (1983) Effects of culture age on symbiotic infectivity of Rhizobium japonicum. J Bacteriol 153: 443–51

    PubMed  CAS  Google Scholar 

  • Bhuvaneswari TV, Turgeon BG, Bauer WD (1980) Early events in the infection of soybean Glycine max (L.) Men. by Rhizobium japonicum. I. Localization of infectible root cells. Plant Physiol 66: 1027–1031

    Google Scholar 

  • Bladergroen MR, Spaink HP (1998) Genes and signal molecules involved in the rhizobiaLeguminoseae symbiosis. Cuff Opin Plant Biol 1: 353–9

    Article  CAS  Google Scholar 

  • Brewin NJ (1991) Development of the legume root nodule. Annu Rev Cell Biol 7:191–226 Broughton WJ, Perret X (1999) Genealogy of legume-Rhizobium symbioses. Curr Opin Plant Bio! 2: 305–11

    Google Scholar 

  • Caetano-Anollés G, Crist-Estes DK, Bauer WD (1988) Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacteriol 170: 31649

    Google Scholar 

  • Caetano-Anollés G, Gresshoff PM (1991) Plant genetic control of nodulation. Annu Rev Microbiol 45: 345–82

    Article  PubMed  Google Scholar 

  • Caetano-Anollés G, Gresshoff PM (1991) Alfalfa controls nodulation during the onset of Rhizobium-induced cortical cell division. Plant Physiol 95: 366–373

    Article  PubMed  Google Scholar 

  • Cassab GI (1998) Plant cell wall proteins. Annu Rev Plant Physiol Plant Mol Biol 49: 281–309

    Article  PubMed  CAS  Google Scholar 

  • Cheng HP, Walker GC (1998) Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J Bacteriol 180: 5183–91

    PubMed  CAS  Google Scholar 

  • Christiansen H, Hansen AC, Vijn I, Pallisgaard N, Larsen K, Yang WC, Bisseling T, Marcker KA, Jensen EO (1996) A novel type of DNA-binding protein interacts with a conserved sequence in an early nodulin ENOD12 promoter. Plant Mol Biol 32: 809–21

    Article  PubMed  CAS  Google Scholar 

  • Cook D, Dreyer D, Bonnet D, Howell M, Nony E, VandenBosch K (1995) Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. Plant Cell 7: 43–55

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13: 171–201

    Article  PubMed  CAS  Google Scholar 

  • Csanddi G, Szecsi J, Kalo P, Kiss P, Endre G, Kondorosi A, Kondorosi E, Kiss GB (1994) ENOD12, an early nodulin gene, is not required for nodule formation and efficient nitrogen fixation in alfalfa. Plant Cell 6: 201–13

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Djordjevic MA, Mathesius U, Arioli T, Weinman JJ, Gaertner E (1997) Chalcone synthase gene expression in transgenic subterranean clover correlates with localised accumulation of flavonoids. Australian Journal of Plant Physiology 24: 119–132

    Article  CAS  Google Scholar 

  • Downie JA, Johnston AW (1986) Nodulation of legumes by Rhizobium: the recognized root? Cell 47: 153–4

    Article  PubMed  CAS  Google Scholar 

  • Duckett CM, Oparka KJ, Prior DAM, Dolan L, Roberts K (1994) Dye-coupling in the root epidermis of Arabidopsis is progressively reduced during development. Development 120: 3247–3255

    CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Erwee MG, Goodwin PB (1985) Symplastic domains in extrastellar tissues of Egeria densa Planch. Planta 163: 9–19

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Felle HH, Kondorosi E, Kondorosi A and 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

    Article  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

    Article  CAS  Google Scholar 

  • Finan TM, Hirsch AM, Leigh JA, Johansen E, Kuldau GA, Deegan S, Walker GC, Signer ER (1985) Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation. Cell 40: 869–77

    Article  PubMed  CAS  Google Scholar 

  • Fisher RF, Long SR (1992) Rhizobium-plant signal exchange. Nature 357: 655–60

    Google Scholar 

  • Galat A, Gerbod M, Bouet F, Riviere S (1996) Proteins and their amino acid compositions: uniqueness, variability, and applications. Arch Biochem Biophys 330: 229–37

    Article  PubMed  CAS  Google Scholar 

  • Gamas P, Niebel FdC, Lescure N, Cullimore J (1996) Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. Mol Plant Microbe Interact 9: 233–42

    Article  PubMed  CAS  Google Scholar 

  • Gloudemans T, Bhuvaneswari TV, Moerman M, Van Brussel T, Van Kammen A, Bisseling T (1989) Involvement of Rhizobium leguminosarum nodulation genes in gene expression in pea root hairs. Plant Mol Biol 12: 157–168

    Article  CAS  Google Scholar 

  • Govers F, Gloudemans T, Moerman M, Van Kammen A, Bisseling T (1985) Expression of plant genes during the development of pea root nodules. EMBO J 4: 861–867

    PubMed  CAS  Google Scholar 

  • Govers F, Harmsen H, Heidstra R, Michielsen P, Prins M, van Kammen A, Bisseling T (1991) Characterization of the pea ENODI2B gene and expression analyses of the two ENOD12 genes in nodule, stem and flower tissue. Mol Gen Genet 228: 160–6

    Article  PubMed  CAS  Google Scholar 

  • Greene EA, Erard M, Dedieu A, Barker DG (1998) MtENOD16 and 20 are members of a family of phytocyanin-related early nodulins. Plant Mol Bio! 36: 775–83

    Article  CAS  Google Scholar 

  • Grosskopf E, Ha DTC, Wingender R, Roehrig H, Szecsi J, Kondorosi E, Schell J, Kondorosi A (1993) Enhanced levels of chalcone synthase in alfalfa nodules induced by a Fix negative mutant of Rhizobium meliloti. Mol Plant Microbe Interact 6: 173–181

    Article  CAS  Google Scholar 

  • Heidstra R, Bisseling T (1996) Nod-factor-induced host responses and mechanisms of Nod-factor perception. New Phytologist 133: 25–43

    Article  CAS  Google Scholar 

  • Heidstra R, Geurts R, Franssen H, Spaink HP, 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, Nilsen G, Martinez-Abarca F, van Kammen A, Bisseling T (1997a) Nod-factorinduced expression of leghemoglobin to study the mechanism of NH4NO3 inhibition on root hair deformation. Mol Plant Microbe Interact 10: 215–20

    Article  PubMed  CAS  Google Scholar 

  • Heidstra R, Yang WC, Yalcin Y, Peck S, Emons AM, van Kammen A, Bisseling T (1997b) 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: 1781–7

    PubMed  CAS  Google Scholar 

  • Hong, JC, Nagao, RT, Key, JL (1990) - Characterization of a proline-rich cell wall protein gene family of soybean. A comparative analysis. J Biol Chem 265: 2470–5

    Google Scholar 

  • Horst J, Stanbro H, Merril CR (1980) On procaryotic gene expression in eucaryotic systems. Hum-Genet 54: 289–302

    Article  PubMed  CAS  Google Scholar 

  • Horvath B, Heidstra R, Lados M, Moerman M, Spaink HP, Prome JC, van Kammen A, Bisseling T (1993) Lipo-oligosaccharides of Rhizobium induce infection-related early nodulin gene expression in pea root hairs. Plant J 4: 727–33

    Article  PubMed  CAS  Google Scholar 

  • Journet EP, Pichon M, Dedieu A, de Billy F, Truchet G, Barker DG (1994) Rhizobium meliloti Nod-factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. Plant J 6: 241–9

    Google Scholar 

  • Jungblut P, Otto A, Zeindl-Eberhart E, Plessner KP, Knecht M, Regitz-Zagrosek V, Fleck E, Wittmann-Liebold B (1994) Protein composition of the human heart: the construction of a myocardial two-dimensional electrophoresis database. Electrophoresis 15: 685–707

    Article  PubMed  CAS  Google Scholar 

  • Kannenberg EL, Brewin NJ (1994) Host-plant invasion by Rhizobium: the role of cell-surface components. Trends Microbiol 2: 277–83

    Article  PubMed  CAS  Google Scholar 

  • Kijne JW (1991) The rhizobium infection process. In: Stacey G, Burris RH and Evans HJ (Eds) Biological Nitrogen Fixation. Chapman and Hall, London, pp 348–397

    Google Scholar 

  • Kozian, Dh, Kirschbaum, Bj (1999) Comparative gene-expression analysis. Trends Biotechnol 17: 73–8

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Leigh JA, Walker GC (1994) Exopolysaccharides of Rhizobium: synthesis, regulation and symbiotic function. Trends Genet 10: 63–7

    Article  PubMed  CAS  Google Scholar 

  • Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome JC, Denarie J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781–4

    Article  PubMed  CAS  Google Scholar 

  • Liang P, Pardee A, (1998) Differential display. A general protocol. Mol Biotechnol 10: 2617

    Google Scholar 

  • Long SR, Staskawicz BJ (1993) Prokaryotic plant parasites. Cell 73: 921–35

    Article  PubMed  CAS  Google Scholar 

  • Martin, Kj, Pardee, Ab (1999)–Principles of differential display. Methods Enzymol 303: 234–58

    Google Scholar 

  • McKhann HI, Pavia NL, Dixon RA, Hirsch AM (1997) Chalcone synthase transcripts are detected in Alfalfa root hairs following inoculation with wild-type Rhizobium meliloti. Mol Plant Microbe Interact 10: 50–58

    Article  CAS  Google Scholar 

  • Mylona P, Moerman M, Yang WC, Gloudemans T, Van de Kerckhove J, van Kammen A, Bisseling T, Franssen HJ (1994) The root epidermis-specific pea gene RH2 is homologous to a pathogenesis-related gene. Plant Mol Bio! 26: 39–50

    CAS  Google Scholar 

  • Nap JP, Bisseling T (1990) Nodulin function and nodulin gene regulation in root nodule development. In: Gresshoff PM (Ed). Molecular biology of symbiotic nitrogen fixation. CRC Press, Inc., Boca Raton, Florida, pp 181–229

    Google Scholar 

  • Otte O, Barz W (1996) The elicitor-induced oxidative burst in cultured chickpea cells drives the rapid insolubilization of two cell wall structural proteins. Planta 200: 238–246

    Article  CAS  Google Scholar 

  • Peng H-M, Dreyer DA, VandenBosch KA, Cook D (1996) Gene structure and differential regulation of the Rhizobium-induced peroxidase gene ripl. Plant Physiol 112: 1437–1446

    Article  PubMed  CAS  Google Scholar 

  • Perlick AM, Puhler A (1993) A survey of transcripts expressed specifically in root nodules of broadbean (Vicia faba L.). Plant Mol Bio! 22: 957–70

    Article  CAS  Google Scholar 

  • Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233: 977–80

    Article  PubMed  CAS  Google Scholar 

  • Phillips DA, Kapulnik Y (1995) Plant isoflavonoids, pathogens and symbionts. Trends Microbiol 3: 58–64

    Article  PubMed  CAS  Google Scholar 

  • Pichon M, Joumet EP, Dedieu A, de Billy F, Truchet G, Barker DG (1992) Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell 4: 1199–211

    Google Scholar 

  • Pingret J-L, Journet E-P, Barker DG (1998) Rhizobium Nod-factor Signaling: Evidence for a G-Protein—Mediated Transduction Mechanism. Plant Cell 10: 659–671

    Google Scholar 

  • Ridge RW, Rolfe BG (1985) Rhizobium sp. degradation of legume root hair cell wall at the site of infection thread origin. Appl Envtl Micro 50: 717–720

    Google Scholar 

  • Roche P, Debelle F, Lerouge P, Vasse J, Truchet G, Prome JC, Denarie J (1992) The lipooligosaccharidic symbiotic signals of Rhizobium meliloti. Biochem Soc Trans 20: 28891

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Scheres B, Van De Wiel C, Zalensky A, Horvath B, Spaink H, Van Eck H, Zwartkruis F, Wolters AM, Gloudemans T et al. (1990a) The ENOD12 gene product is involved in the infection process during the pea Rhizobium interaction. Cell 60: 281–294

    Article  PubMed  CAS  Google Scholar 

  • Scheres B, Van Engelen F, Van Der Knaap E, Van De Wiel C, Van Kammen A, Bisseling T (1990b) Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell 2: 687–700

    Article  PubMed  CAS  Google Scholar 

  • Schultze M, Kondorosi A (1995) What makes nodulation signals host-plant specific? Trends Microbiol 3: 370–2

    Article  PubMed  CAS  Google Scholar 

  • Schultze M, Kondorosi A (1998) Regulation of symbiotic root nodule development. Annu Rev Genet 32: 33–57

    Article  PubMed  CAS  Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5: 9–23

    Article  PubMed  CAS  Google Scholar 

  • Sieberer B and AMC Emons (2000) Cytoarchitecture and pattern of cytoplasmic streaming in developing root hairs of Medicago truncatula and during deformation by Nod-factors. Protoplasma, submitted

    Google Scholar 

  • Snehal P, Poornima I, Vaishali G, Trilok P, Anjana D, Pandya S, Iyer P, Gaitonde V, Parekh T, Desai A (1999) Chemotaxis of Rhizobium SP.S2 towards Cajanus cajan root exudate and its major components. Current Microbiology 38: 205–209

    Article  Google Scholar 

  • Timmers AC, Auriac MC, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126: 3617–3628

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Turgeon BG, Bauer WD (1985) Ultrastructure of infection-thread development during the infection of soybean by Rhizobium japonicum. Planta 163: 328–349

    Article  Google Scholar 

  • Vijn I, Christiansen H, Lauridsen P, Kardailsky I, Quandt HJ, Broer I, Drenth J, Ostergaard Jensen E, van Kammen A, Bisseling T (1995a) A 200 bp region of the pea ENOD12 promoter is sufficient for nodule-specific and Nod-factor induced expression. Plant Mol Biol 28: 1103–10

    Article  PubMed  CAS  Google Scholar 

  • Vijn I, Martinez-Abarca F, Yang WC, das Neves L, van Brussel A, van Kammen A, Bisseling T (1995b) Early nodulin gene expression during Nod-factor-induced processes in Vicia sativa. Plant J 8: 111–9

    Article  PubMed  CAS  Google Scholar 

  • Vijn I, Yang WC, Pallisgard N, Ostergaard Jensen E, van Kammen A, Bisseling T (1995c) VsENOD5, VsENOD12 and VsENOD40 expression during Rhizobium-induced nodule formation on Vicia sativa roots. Plant Mol Biol 28: 1111–9

    Article  PubMed  CAS  Google Scholar 

  • Wilkins MR, Pasquali C, Appel RD, Ou K, Golaz O, Sanchez JC, Yan JX, Gooley AA, Hughes G, Humphery-Smith I, Williams KL, Hochstrasser DF (1996) From proteins to proteomes: large scale protein identification by two-dimensional electrophoresis and amino acid analysis. Biotechnology 14: 61–5

    Article  PubMed  CAS  Google Scholar 

  • Wingender R, Rohrig H, Horicke C, Wing D, Schell J (1989) Differential regulation of soybean chalcone synthase genes in plant defence, symbiosis and upon environmental stimuli. Mol Gen Genet 18: 315–22

    Article  Google Scholar 

  • Wojtaszek P, Trethowan J, Bolwell GP (1997) Reconstitution in vitro of the components and conditions required for the oxidative cross-linking of extracellular proteins in French bean (Phaseolus vulgaris L.). FEBS Letters 405: 95–980

    Article  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

Jahraus, A., Bisseling, T. (2000). Rhizobium-Induced Plant Gene Expression in 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_16

Download citation

  • DOI: https://doi.org/10.1007/978-4-431-68370-4_16

  • 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