Skip to main content

Root Hair-Frankia Interactions in Actinorhizal Symbioses

  • Chapter
Root Hairs

Abstract

The term actinorhizae refers to the nitrogen-fixing nodular structures induced on roots of higher plants by the actinomycete Frankia (Tjepkema and Torrey 1979). Occurrence of actinorhizal nodules is reported for about 200 different plant species from 23 genera distributed over eight dicotyledonous families (Table 1; van Ghelue 1994). Except for the genus Datisca, all other actinorhizal hosts are woody shrubs and their geographical distribution is primarily temperate. Only some hosts of the families Casuarinaceae and Myricaceae are tropical. Actinorhizal plants possess great economic value as timber and fuel wood. They are also used extensively in land reclamation and as ornamental shrubs. Ecologically, actinorhizal plants are pioneer invaders of nitrogen poor sites (Baker and Schwintzer 1990).

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.

References

  • Baker DD and Schwintzer CR (1990) Introduction. In: Schwintzer CR and Tjepkema JD (Eds) The biology of Frankia and Actinorhizal Plants. Academic press, New York. pp 3–11

    Google Scholar 

  • Benoit LF and Berry AM (1997) Flavonoid-like compounds from seeds of red alder (Alnus rubra) influence host nodulation by Frankia (Actinomycetales). Physiol Plant 99:588–593

    Google Scholar 

  • Berry AM and McCully ME (1990) Callose-containing deposits in relation to root-hair infections of Alnus rubra by Frankia. Can J Bot 68: 798–802

    Article  Google Scholar 

  • Berry AM, McIntyre L and McCully ME (1986) Fine structure of root hair infection leading to nodulation in the Frankia Alnus symbiosis. Can J Bot 64: 292–305

    Article  Google Scholar 

  • Berry AM and Sunell LA (1990) The infection process and nodule development. In: Schwintzer CR and Tjepkema JD (Eds) The Biology of Frankia and Actinorhizal plants. Academic Press Inc., New York.pp 61–81

    Google Scholar 

  • Berry AM and Torrey JG (1983) Root hair deformation in the infection process of Alnus rubra. Can J Bot 61: 2863–2876

    Article  Google Scholar 

  • Berry AM, Torrey JG and McCully ME (1983) The fine structure of the root hair wall and surface mucilage in the actinorhizal host Alnus rubra. In: Goldberg R (Ed) Plant Molecular Biology Alan R. Liss inc, New York. pp 319–327

    Google Scholar 

  • Bhuvaneswari TV and Solheim B (1985) Root hair deformation in the white clover (Trifolium repens) and Rhizobium trifolii symbiosis. Physiol Plant 63: 25–34

    Article  CAS  Google Scholar 

  • Burggraaf AJP, van der Linden J and Tak T (1983) Studies on the localization of infectable cells on Alnus glutinosa roots. Plant Soil 74: 175–188

    Article  Google Scholar 

  • Callaham D, Newcomb W, Torrey JG and Peterson RL (1979) Root hair infection in actinomycete-induced root nodule initiation in Casuarina, Myrica, aND Comptonia. Bot Gaz 140:S1- S9

    Google Scholar 

  • Callaham D, Tredici PD and Torrey JG (1978) Isolation and cultivation in vitro of the actinomycete causing rot nodulation in Comptonia. Science (Washington) 199: 899–902

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Carmona AF (1974) La formation des nodule fixateurs d’azote chez Alnus glutinosa (L.) Vill. Acta Bot Ned 23: 257–303

    Google Scholar 

  • Chen L-M, Cui Y-H, Qin M, Wang Y-l, Bai X-l and Ma Q-S (1991) Identification of a nodD -like gene in Frankia by direct complementation of a Rhizobium nodD- mutant. Mol Gen Genet 233: 311–314

    Google Scholar 

  • Cheng HP and 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 

  • Cournoyer B, Gouy M and Normand P (1993) Molecular phylogeny of the symbiotic actinomycetes of the genus Frankia matches host-plant infection processes. Mol Biol Evol 10: 1303–1316

    PubMed  CAS  Google Scholar 

  • Dawes CJ and Bowler E (1959) Light and electron microscope studies of the cell wall structure of the root hairs of Rhaphanus sativus. Am. J. Bot. 46: 561–565

    Article  Google Scholar 

  • Dénarié J, Debellé F and Rosenberg C (1992) Signaling and host range in nodulation. Annu Rev Microbiol 46: 497–531

    Article  PubMed  Google Scholar 

  • Djordjevic MA, Redmond JW, Bately M and Rolfe BG (1987) Clovers secrete specific compounds which stimulate or repress nod gene expression in Rhizobium trifolii. EMBO J 6: 1173–1179

    PubMed  CAS  Google Scholar 

  • Doyle JJ (1998) Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci 3: 473–478

    Article  Google Scholar 

  • Gresshoff PM, Mathews A, Krotsky A, Olsson JE, Carroll BJ, Delvis AC, Kosslak R, Applebaum ER and Day DA (1988) Supernodulation and non-nodulation mutants of soybean. In: Palacios R and Verma DPS (Eds) Molecular genetics of Plant-microbe Interactions. APS press St. Paul, MN pp 364–369

    Google Scholar 

  • Heidstra R, Geurts R, Franssen H, Spaink HP, van Kammen A and 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 

  • Hirsch AM and LaRue TA ( 1997 Is the legume nodule a modified root or stem organ or an organ sui generis? Critical Reviews in Plant Science 16: 361–392

    Google Scholar 

  • Knowlton S, Berry A and Torrey JG (1980) Evidence that associated soil bacteria may influence root hair infection of actinorhizal plants by Frankia. Can J Microbiol 26: 971–977

    Article  PubMed  CAS  Google Scholar 

  • Krishnan HB and Pueppke SG (1994) A cloned cellulase gene from Erwinia carotovora subsp. carotovora is expressed in Rhizobium fredii but does not influence nodulation of cowpea. FEMS Microbiol Lett 119: 289–294

    CAS  Google Scholar 

  • Lalonde M (1977) The infection process of Alnus root nodule symbiosis. In Recent Developments in Nitrogen fixation. Newton W, Postgate JR and.Rodriguez-Barrueco C (Eds) Academic Press New York pp 569–589

    Google Scholar 

  • Liu Q and Berry AM (1991) Localization and characterization of pectic polysaccharides in roots and root nodules of Ceanothus spp. during intercellular infection by Frankia. Protoplasma 163: 93–101

    Article  CAS  Google Scholar 

  • Long SR (1989) Rhizobium-legume nodulation: Life together in the underground. Cell 56:203–214

    Google Scholar 

  • Maggia L and Bousquet J (1994) Molecular phylogeny of the actinorhizal Hamamelidae and relationships with host promiscuity towards Frankia. Mol Ecol 3: 459–467

    Article  Google Scholar 

  • Mateos FM, Jimenez-Zuro JI, Chen J, Squartini AS, Haack SK, Martinez-Molina E, Hubbel DH and Dazzo FB (1992) Cell-associated pectinolytic and cellulolytic enzymes in Rhizobium leguminosarum biovar trifolii. Appl. Environ. Microbiol. 58: 1816–1822

    Google Scholar 

  • Miller IM and Baker DD (1985) The initiation, development and structure of root nodules in Elaeagnus angustifolia (Elaeagnaceae). Protoplasma 128: 107–119

    Article  Google Scholar 

  • Miller IM and Baker DD (1986) Nodulation of actinorhizal plants by Frankia strains capable of both root hair infection and intercellular penetration. Protoplasma 131:

    Google Scholar 

  • Munoz, JA, Coronado, C, Perez-Hormaeche, J, Kondorosi, A, Ratet, P, and Palomares,AJ (1998) MsPG3, a Medicago sativa polygalacturonase gene expressed during the alfalfa-Rhizobium meliloti interaction PNAS 95: 9687–9692

    CAS  Google Scholar 

  • Pawlowski K (1997) Nodule-specific gene expression. Physiol Plant 99: 617–631

    Article  CAS  Google Scholar 

  • Pawlowski K and Bisseling T (1996) Rhizobial and actinorhizal symbioses: What are the shared features? Plant Cell 8: 1899–1913

    Article  PubMed  CAS  Google Scholar 

  • Penmetsa RV and Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science (Washington) 275: 527–530

    Article  CAS  Google Scholar 

  • Prin Y and Rougier M (1986) Cytological and histochemical characteristics of the axenic root surface of Alnus glutinosa. Can J Bot 64: 2216–2226

    Article  Google Scholar 

  • Prin Y and Rougier M (1987) Preinfection events in the establishment of Alnus- Frankia Symbiosis: Study of root hair deformation step. Plant Physiology (Life SciAdv) 6: 99–106

    Google Scholar 

  • Quispel A (1990) Discoveries, discussions and trends in research on actinorhizal root nodule symbioses before 1978. In: Schwintzer CR and Tjepkema JD (Eds) The Biology of Frankia and Actinorhizal plants Academic Press Inc New York. pp 17–28

    Google Scholar 

  • Racette S and Torrey JG (1989) Root nodule initiation in Gymnostoma (Casuarinaceae) and Shepherdia (Elaeagnaceae) induced by Frankia strain HFPGpI 1. Can J Bot 67: 2873–2879

    Article  Google Scholar 

  • Rasmussen U, Johansson C, Renglin A, Petersson C and Bergman B (1996) A molecular characterization of the Gunnera-Nostoc symbiosis: comparison with Rhizobium and Agrobacterium plant interactions. New Phytol 133: 391–398

    Article  CAS  Google Scholar 

  • Reddy A, Bochenek B and Hirsch AM (1992) A new Rhizobium meliloti symbiotic mutant isolated after introducing Frankia DNA sequence into a nodA::Tn5 strain. Mol Plant Micro Inter 5: 62–71

    Article  CAS  Google Scholar 

  • Ringo E, Clausen E, Lovaas E, van Ghelue M and Solheim B (1995) Effects of extracts of Alnus glutinosa seeds on growth of Frankia strain ArI3 under static and fermentor culture conditions. Plant Soil 176: 283–288

    Article  Google Scholar 

  • Roche P, Lerouge P, Ponthus C and Prome JC (1991) Structural determination of bacterial nodulation factors involved in the Rhizobium meliloti alfalfa symbiosis. J Biol Chem 266: 10933–10940

    PubMed  CAS  Google Scholar 

  • Safo Sampah S and Torrey JG (1988) Polysaccharide-hydrolyzing enzymes of Frankia (Actinomycetales). Plant Soil 112: 89–98

    Article  CAS  Google Scholar 

  • Schwencke J and Selim S (1995) Deformation factors of Casuarina root hairs (dnF) are induced in Frankia by flavonoids from Casuarina seeds. In: Berry AM (Ed) 10th international conference on Frankia and actinorhizal plants. University of California, Davis.

    Google Scholar 

  • Seguin A, Lalonde M, Winship LJ and Benson DR (1989) Detection of pectolytic activity and pel homologous sequences in Frankia. Plant Soil 118: 1–2

    Article  Google Scholar 

  • Spaink HP and Lugtenberg BJJ (1994) Role of rhizobial lipo-chitin oligosaccharide signal molecules in root nodule organogenesis. Plant Mol Biol 26: 1413–1422

    Article  PubMed  CAS  Google Scholar 

  • Spaink, HP, Sheeley, D.M, van Brussel, AA, Glushka, J, York W S, Tak, T, Geiger O, Kennedy EP, Reinhold V, and Lugtenberg BJ (1991) A novel highly unsaturated fatty acid moiety of lipo-ologosaccharide signal determines host specificity of Rhizobium. Nature 328: 337–340

    Article  Google Scholar 

  • Sprent JI (1994) Evolution and diversity in the legume-Rhizobium symbioses: Chaos theory? Plant Soil 161: 1–10

    Article  Google Scholar 

  • Sprent JI, Sutherland JM, F, De Faria SM, Stirton CH and Zarucchi JL (1989) Structure and function of root nodules from woody legumes. Advances in legume biology Monographs in Systematic Botany from the Missouri Botanical Garden 29: 559–578

    Google Scholar 

  • Swensen SM and Mullin BC (1997) Phylogenetic relationships among actinorhizal plants: The impact of molecular systematics and implications for the evolution of actinorhizal symbiosis. Physiol Plant 99: 565–573

    Article  CAS  Google Scholar 

  • Tjepkema JD and Torrey JG (1979) Symbiotic nitrogen fixation in actinomycete-nodulated plants. Bot Gaz (supplement) 140:i-ii

    Google Scholar 

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

    CAS  Google Scholar 

  • van Brussel AAN, Bakhuizen R, van Spronsen PC, Spaink HP, Tak T, sLugtenberg BJJ and Kijne JW (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science (Washington) 257: 70–72

    Article  Google Scholar 

  • van Ghelue M (1994) Interactions in Actinorhizal symbiosis. Thesis, University of Tromso.

    Google Scholar 

  • van Ghelue M, Lovaas E, Ringo E and Solheim B, (1995) Early interactions between Alnus glutinosa and Frankia strain ArI3. Production and specificity of root hair deformation factor(s). Physiol Plant 99: 579–587

    Google Scholar 

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

    Google Scholar 

  • van Workum W. A.T, van Slageren Sophie, van Brussel AAN and Kijne JW (1998) Role of exopolysaccharides of Rhizobium leguminosarum by. viciae as host plant -specific molecules required for infection thread formation during nodulation of Vicia sativa. Mol Plant Micro Inter 11: 1233–1241

    Article  Google Scholar 

  • Wall LG and Huss Danell K (1997) Regulation of nodulation in Alnus incana-Frankia symbiosis. Physiol Plant 99: 594–600

    Article  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

Bhuvaneswari, T.V., Solheim, B. (2000). Root Hair-Frankia Interactions in Actinorhizal Symbioses. In: Ridge, R.W., Emons, A.M.C. (eds) Root Hairs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-68370-4_18

Download citation

  • DOI: https://doi.org/10.1007/978-4-431-68370-4_18

  • 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