Skip to main content

Infection of Root Hairs by Rhizobia: Infection Thread Development with Emphasis on the Microtubular Cytoskeleton

  • Chapter
Root Hairs

Abstract

The symbiotic interaction between soil bacteria of the genera Rhizobium, Azorhizobium or Bradyrhizobium (generally referred to as rhizobia) and plants of the Leguminosae family result in the formation of nodules, new organs in which the bacteria reduce nitrogen into ammonia which can subsequently be utilized by the plant (for reviews on nodulation see Mylona et al. 1995; Dénarié et al. 1996; Long 1996; Hirsch and LaRue 1997). In a large number of interactions bacterial infection takes place through the development of an infection thread in root hairs of the host plant (reviewed by Kijne 1992). In this chapter I will first briefly describe the growth and structure of root hairs and recapitulate the relevant aspects of the infection process before going into detail of the changes in the organization of the microtubular cytoskeleton in root hairs during infection with rhizobia.

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 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

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  • Aist JR (1976) Papillae and related wound plugs of plant cells. Annu Rev Phytopathol 14: 145–163

    Article  Google Scholar 

  • Aoyama T, Chua N-H (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11: 605–612

    Article  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 

  • Bakhuizen R (1988) The plant cytoskeleton in the Rhizobium-legume symbiosis. PhD thesis. Leiden University, The Netherlands

    Google Scholar 

  • Baluska F, Parker JS, Barlow PW (1992) Specific patterns of cortical and endoplasmic microtubules associated with cell growth and tissue differentiation in roots of maize (Zea mays L.). J Cell Sci 103: 191–200

    Google Scholar 

  • Belford DS, Preston RD (1961) The structure and growth of root hairs. J Exp Bot 12: 157168

    Google Scholar 

  • Bénaben V, Duc G, Lefebvre V, Huguet T (1995) TE7, an inefficient symbiotic mutant of Medicago truncatula Gaertln. Cv Jemalong. Plant Physiol 107: 53–62

    PubMed  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, Turgeon G, Bauer W (1980) Early events in the infection of soybean (Glycine max L. Merr) by Rhizobium japonicum. Plant Physiol 66: 1027–1031

    Article  PubMed  CAS  Google Scholar 

  • Bibikova T, Zhigilei A, Gilroy S (1997) Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203: 495–505

    Article  PubMed  CAS  Google Scholar 

  • Callaham DA, Torrey JG (1981) The structural basis for infection of root hairs of Trifolium repens by Rhizobium. Can J Bot 59: 1647–1664

    Article  Google Scholar 

  • Calvert HE, Pence MK, Pierce M, Malik NSA, Bauer WD (1984) Anatomical analysis of the development and distribution of Rhizobium infections in soybean roots. Can J Bot 30: 2375–2384

    Article  Google Scholar 

  • Cocking E (1985) Protoplasts from root hairs of crop plants. Bio/Technol 3:1104–1106 Cormack RGH (1962) Development of root hairs in angiosperms. II. Bot Rev 28: 446–464

    Google Scholar 

  • Dart PJ (1974) The infection process. In: Quispel A (ed) The biology of nitrogen fixation. North-Holland, Amsterdam, pp 381–429

    Google Scholar 

  • Dazzo FB, Orgamide GG, Philip-Hollingsworth S, Hollingsworth RI, Ninke KO, Salzwedel JL (1996) Modulation of development, growth dynamics, wall crystallinity, and infection sites in white clover root hairs by membrane chitolipooligosaccharides from Rhizobium leguminosarum biovar trifolii. J Bacteriol 178: 3621–3627

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Diaz CD, van Spronsen PC, Bakhuizen R, Logman GJJ, Lugtenberg EJJ, Kijne JW (1986) Correlation between infection by Rhizobium leguminosarum and lectin on the surface of Pisum sativum L. roots. Planta 168: 350–359.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Dolan L, Duckett C, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K (1994) Clonal relationship and cell patterning in the root epidermis of Arabidopsis. Development 120: 2465–2474

    CAS  Google Scholar 

  • Emons AMC, Derksen J, Sassen MMA (1992) Do microtubules control plant cell wall microfibrils? Physiol Plant 84: 486–493

    Article  CAS  Google Scholar 

  • Felle HH, Hepler PK (1997) The cytosolic Cat* concentration gradient of Sinapis alba root hairs as revealed by Cat+-selective microelectrode tests and Fura-dextran ratio imaging. Plant Physiol 114: 39–45

    PubMed  CAS  Google Scholar 

  • Gage DJ, Bobo T, Long SR (1996) Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and Alfalfa (Medicago sativa). J Bacteriol 178: 7159–7166

    PubMed  CAS  Google Scholar 

  • Goodchild DJ, Bergersen FJ (1966) Electron microscopy of the infection and subsequent development of soybean nodule cells. J Bacteriol 92: 204–213

    PubMed  CAS  Google Scholar 

  • Griffin BA, Adams SR, Tsien RY (1998) Specific covalent labeling of recombinant protein molecules inside live cells. Science 281: 269–272

    Article  PubMed  CAS  Google Scholar 

  • Halverson U, Stacey G (1986) Signal exchange in plant-microbe interactions. Microbiol Rev 50: 193–225

    PubMed  CAS  Google Scholar 

  • Hasezawa S, Sano T, Nagata T (1998) The role of microfilaments in the organization and orientation of microtubules during the cell cycle transition from M Phase to Gl phase in tobacco BY-2 cells. Protoplasma 202: 105–114

    Article  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 

  • Hepler PK, Gunning BES (1998) Confocal fluorescence microscopy of plant cells. Protoplasma 201: 121–157

    Article  Google Scholar 

  • Higashi S, Abe M (1980) Scanning electron microscopy of Rhizobium trifolii infection sites on root hairs of white clover. Appl Environ Microbiol 40: 1094–1099

    PubMed  CAS  Google Scholar 

  • Higashi S, Kushiyama K, Abe M. (1987) Electron microscopic observations of infection threads in driselase treated nodules of Astragalus sinicus. Can. J. Microbiol. 32: 947–952.

    Google Scholar 

  • Hirsch AM, LaRue TA (1997) Is the legume nodule a modified root or stem or an organ sui generis? Crit Rev Plant Sci 16: 361–392

    Google Scholar 

  • Hubbel DH (1981) Legume infection by Rhizobium: A conceptual approach. BioScience 31: 832–837

    Google Scholar 

  • Katz B-Z, Krylov D, Aota S-i, Olive M, Vinson C, Yamada KM (1998) Green fluorescent protein labeling of cytoskeletal structures-Novel targeting approach based on leucine zippers. BioTechniques 25: 298–304

    CAS  Google Scholar 

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

    Google Scholar 

  • Kobayashi Y, Kobayashi I, Funaki Y, Fujimoto S, Takemoto T, Kunoh H (1997) Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J 11: 525–537

    Article  CAS  Google Scholar 

  • Leffel SM, Mabon SA, Stewart CN (1997) Applications of green fluorescent protein in plants. BioTechniques 23: 912–918

    CAS  Google Scholar 

  • Libbenga KR, Harkes PAA (1973) Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L. Planta 114: 17–28

    Article  Google Scholar 

  • Libbenga KR, Bogers RJ (1974) Root-nodule morphogenesis. In: Quispel A (Ed) The biology of nitrogen fixation. North-Holland, Amsterdam, pp 430–472

    Google Scholar 

  • Lillich TT, Elkan GH (1968) Evidence countering the role of polygalacturonase in invasion of root hairs of leguminous plants by Rhizobium spp. Can J Microbiol 14: 617–625

    Article  PubMed  CAS  Google Scholar 

  • Ljunggren H, Fahraeus G (1961) The role of polygalacturonase in root hair invasion by nodule bacteria. J Gen Microbiol 26: 521–528

    PubMed  CAS  Google Scholar 

  • Lloyd CW, Pearce KJ, Rawlins DJ, Ridge RW, Shaw P (1987) Endoplasmic microtubules connect the advancing nucleus to the tip of legume root hairs, but F-actin is involved in basipetal migration. Cell Motil Cytoskeleton 8: 27–36

    Article  Google Scholar 

  • Long SR (1996) Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885–1898 Ludin B, Matus A (1998) GFP illuminates the cytoskeleton. Trends Cell Biol 8:72–77

    Google Scholar 

  • Marc J, Granger CL, Brincat J, Fisher DD, Kao T-h, McCubbin AG, Cyr RJ (1998) A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. Plant Cell 10: 1927–1939

    Article  PubMed  CAS  Google Scholar 

  • Miller DD, de Ruijter NCA, 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 

  • Mort AJ, Grover PB (1988) Characterization of root hair cell walls as potential barriers to the infection of plants by rhizobia. Plant Physiol 82: 787–794

    Google Scholar 

  • Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. Plant Cell 7: 869–885

    Article  PubMed  CAS  Google Scholar 

  • Napoli CA, Hubbell DH (1975) Ultrastructure of Rhizobium-induced infection threads in clover root hairs. Appl Microbiol 30: 1003–1009

    PubMed  CAS  Google Scholar 

  • Newcomb W (1981) Nodule morphogenesis and differentiation. In: Giles KL, Atherly AG (Eds) Biology of the Rhizobiaceae. Int Rev Cytol suppl 13. Academic Press, New York, pp 247–298

    Google Scholar 

  • Newcomb W, Sippell D, Peterson RL (1979) The early morphogenesis of Glycine max and Pisum sativum root nodules. Can J Bot 57: 2603–2616

    Article  Google Scholar 

  • Nutman PS (1959) Some observations on root hair infection by nodule rhizobia. J Exp Bot 10: 250–263

    Article  Google Scholar 

  • Rae AL, Bonfante-Fasolo P, Brewin NJ (1992) Structure and growth of infection threads in the legume symbiosis with Rhizobium leguminosarum. Plant J 2: 385–395

    Article  Google Scholar 

  • Ridge RW (1990) Cytochalasin-D causes abnormal wall-ingrowths and organelle-crowding in legume root hairs. Bot Magazine Tokyo 103: 87–96

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Ridge RW (1995) Recent developments in the cell and molecular biology of root hairs. J Plant Res 108: 399–405

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Robertson JG, Lyttleton P (1982) Coated and smooth vesicles in the biogenesis of cell walls, plasma membranes, infection threads and peribacteroid membranes in root hairs and nodules of white clover. J Cell Sci 58: 63–78

    PubMed  CAS  Google Scholar 

  • Row HC, Reeder JR (1957) Root hair development as evidence of relationship among genera of Gramineae. Am J Bot 44: 596–601

    Article  Google Scholar 

  • Sagan M, Huguet T, Duc G (1994) Phenotypic characterization and classification of nodulation mutants of pea (Pisum sativum L.). Plant Sci 100: 59–70

    Article  CAS  Google Scholar 

  • Sahlman K, Fahraeus G (1963) An electron microscope study of root-hair infection by Rhizobium. J Gen Microbiol 33: 425–427

    PubMed  CAS  Google Scholar 

  • Schnall JA, Quatrano RS (1992) Abscisic acid elicits the water stress response in root hairs of Arabidopsis thaliana. Plant Physiol 100: 216–218

    Article  PubMed  CAS  Google Scholar 

  • Seagull RW (1983) The role of the cytoskeleton during oriented microfibril deposition. I Elucidation of the possible interaction between microtubules and cellulose synthetic complexes. J Ultrastruct Res 83: 168–175

    Article  PubMed  CAS  Google Scholar 

  • Sprent JI (1989) Which steps are essential for the formation of functional legume nodules? New Phytol 111: 129–153

    Article  Google Scholar 

  • Sprent JI, Faria SM (1988) Mechanisms of infection of plants by nitrogen fixing organisms. Plant Soil 110: 157–165

    Article  Google Scholar 

  • Timmers ACJ, Auriac M-C, de Billy F, Truchet G (1998) Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development 125: 339–349

    PubMed  CAS  Google Scholar 

  • Timmers ACJ, Auriac M-C, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubule cytsokeletal rearrangements. Development 126: 3617–3628

    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

    Article  CAS  Google Scholar 

  • Traas JA, Braat P, Emons AMC, Meekes H, Derksen J (1985) Microtubules in root hairs. J Cell Sci 76: 303–320

    PubMed  CAS  Google Scholar 

  • Tsien RY (1998) The green fluorescent protein. Annu Rev Biochem 67: 509–544

    Article  PubMed  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 

  • Utrup LJ, Cary AJ, Norris JH (1993) Five nodulation mutants of white sweetclover (Melilotus alba Desr.) exhibit distinct phenotypes blocked at root hair curling, infection thread development, and nodule organogenesis. Plant Physiol 103: 925–932

    PubMed  Google Scholar 

  • van Batenburg FHD, Jonker R, Kijne JW (1986) Rhizobium induces marked root hair curling by redirection of tip growth: a computer simulation. Physiol Plant 66: 476–480

    Google Scholar 

  • van Spronsen PC, Bakhuizen R, van Brussel AAN, 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 

  • Vandenbosch KA, Bradley DJ, Knox JP, Perotto S, Butcher GW, Brewin NJ (1989) Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. EMBO J 8: 335–342

    PubMed  CAS  Google Scholar 

  • Vitha S, Baluska F, Mews M, Volkmann D (1997) Immunofluorescence detection of F-actin on low melting point wax sections from plant tissues. J Histochem Cytochem 45: 89–95

    Article  PubMed  CAS  Google Scholar 

  • Wood SM, Newcomb W (1989) Nodule morphogenesis: The early infection of alfalfa (Medicago sativa) root hairs by Rhizobium meliloti. Can J Bot 67: 3108–3122

    Article  Google Scholar 

  • Wymer C, Lloyd C (1996) Dynamic microtubules: implications for cell wall patterns. Trends Plant Sci 1: 222–228

    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

Timmers, A.C.J. (2000). Infection of Root Hairs by Rhizobia: Infection Thread Development with Emphasis on the Microtubular Cytoskeleton. In: Ridge, R.W., Emons, A.M.C. (eds) Root Hairs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-68370-4_14

Download citation

  • DOI: https://doi.org/10.1007/978-4-431-68370-4_14

  • 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