Skip to main content
Log in

The infection process and nodule initiation in theFrankia-Ceanothus root nodule symbiosis

A structural and histochemical study

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Root nodules are induced in actinorhizal plants by the nitrogen-fixing actinomyceteFrankia. Nodules may be initiated by root hair infection or by intercellular penetration. InCeanothus spp. (Rhamnaceae),Frankia colonized the host root tissue by intercellular infection, in spite of the occurrence of root hairs in the infected region. The intercellular infection pathway was characterized by an extensive darkly-staining matrix which filled prominent intercellular spaces of the root cortex, gradually decreasing through a transition zone into the nodule cortex. At the ultrastructural level, most of the matrix was composed of fibrillar electron dense material. Holes or spaces occurred in the electron dense matrix, often in conjunction with apparent loosening of wall layers. Secondary cell division was observed within the root cortical cells embedded in the intercellular matrix. Unusually high levels of pectic compounds and proteins were identified histochemically in the matrix.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baker DD, Schwintzer CR (1990) Introduction. In: Schwintzer CR, Tjepkema JD (eds) The biology ofFrankia and actinorhizal plants. Academic Press, San Diego, pp 1–13

    Google Scholar 

  • Becking JH (1975) Root nodules in nonlegumes. In: Torrey JG, Clarkson DT (eds) Development and function of roots. Academic Press, London, pp 508–566

    Google Scholar 

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

    Google Scholar 

  • —, Kahn RKS, Booth MC (1989) Identification of indole compounds secreted byFrankia HFPAr13 in defined culture medium. Plant Soil 118: 205–209

    Google Scholar 

  • Callaham D, Torrey JG (1977) Prenodule formation and primary nodule development in roots ofComptonia (Myricaceae). Can J Bot 51: 2306–2318

    Google Scholar 

  • —, Newcomb W, Torrey JG, Peterson RL (1979) Root hair infection in actinomycete-induced root nodule initiation inCasuarina, Myrica andComptonia. Bot Gaz 140 [Suppl]: S 1-S 9

    Google Scholar 

  • Chandler MR (1978) Some observations of infection ofArachis hypogaea byRhizobium. J Exp Bot 29: 749–755

    Google Scholar 

  • —, Date RA, Roughley RJ (1982) Infection and root nodule development inStylosanthes species byRhizobium. J Exp Bot 33: 47–57

    Google Scholar 

  • Clarke A, Gleeson P, Harrison S, Knox RB (1979) Pollen-stigma interactions: identification and characterization of surface components with recognition potential. Proc Natl Acad Sci 76: 3358–3362

    Google Scholar 

  • Foster RC (1982) The fine structure of epidermal cell mucilages of roots. New Phytol 91: 727–740

    Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. University of California Agricultural Experimental Station Circular #347

  • Lancelle SA, Torrey JG (1984) Early development ofRhizobium-induced nodules ofParasponia rigida. I. Infection and early nodule initiation. Protoplasma 123: 26–37

    Google Scholar 

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

    Google Scholar 

  • Miki NK, Clarke KJ, McCully ME (1980) A histological and histochemical comparison of the mucilages on the root tips of several grasses. Can J Bot 58: 2581–2593

    Google Scholar 

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

    Google Scholar 

  • — — (1986) Nodulation of actinorhizal plants byFrankia strains capable of both root hair infection and intercellular penetration. Protoplasma 131: 82–91

    Google Scholar 

  • Newcomb W (1981) Nodule morphogenesis and differentiation. Int Rev Cytol [Suppl] 13: 247–297

    Google Scholar 

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

    Google Scholar 

  • O'Brien TP, McCully ME (1981) The study of plant structure: principles and selected methods. Termarcarphi Pty, Melbourne

    Google Scholar 

  • Racette S, Torrey JG (1989) Root nodule initiation inGymnostoma (Casuarinaceae) andShepherdia (Elaeagnaceae) induced byFrankia strain HFPGpll. Can J Bot 67: 2873–2879

    Google Scholar 

  • Rensselaer MV, McMinn HE (1942) Ceanothus. Gillick Press, Berkeley, CA

    Google Scholar 

  • Sanders LC, Lord EM (1989) Directed movement of latex particles in the gynoecia of three species of flowering plants. Science 243: 1606–1608

    Google Scholar 

  • Séguin A, Lalonde M (1989) Detection of pectolytic activity andpec homologous sequences inFrankia. Plant Soil 118: 221–229

    Google Scholar 

  • Sexton R, Burdon JN, Reid SG, Durbin ML, Lewis LN (1984) Cell wall breakdown and abscission. In: Dugger WR, Bartinicki-Garcia S (eds) Structure, function and biosynthesis of plant cell walls. Waverly Press, Baltimore, MD, pp 195–221

    Google Scholar 

  • Stevens GA, Berry AM (1988) Cytokinin secretion byFrankia sp. HFPArl3 in defined medium. Plant Physiol 87: 15–16

    Google Scholar 

  • Strand R, Laetsch WM (1977 a) Cell and endophyte of the nitrogenfixing root nodules ofCeanothus integerrimus H. and A. I. Fine structure of the nodule and its endosymbiont. Protoplasma 93: 165–178

    Google Scholar 

  • — — (1977 b) Cell and endophyte structure of the nitrogen-fixing root nodules ofCeanothus integerrimus H. and A. II. Progress of the endophyte into young cells of the growing nodule. Protoplasma 93: 179–190

    Google Scholar 

  • Takhtajan A, Jeffrey C (1969) Flowering plants: origin and dispersal. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Thomas BA, Spicer RA (1987) The evolution of modern vegetation. In: Dudley TR (ed) The evolution and palaeobiology of land plants. Dioscorides Press, Portland, OR, pp 267–276

    Google Scholar 

  • Torrey JG (1976) Initiation and development of root nodules ofCasuarina (Casuarinaceae). Amer J Bot 63: 335–344

    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

    Google Scholar 

  • Webster BD (1970) A morphogenetic study of leaf abscission inPhaseolus. Amer J Bot 75: 443–451

    Google Scholar 

  • — (1973) Ultrastructural studies of abscission inPhaseolus: ethylene effects on cell walls. Amer J Bot 60: 436–447

    Google Scholar 

  • Wiatr SM (1978) Physiology and ultrastructure of petal abscission in western blue flax (Linum lewisii). PhD dissertation, University of California, Davis, CA

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, Q., Berry, A.M. The infection process and nodule initiation in theFrankia-Ceanothus root nodule symbiosis. Protoplasma 163, 82–92 (1991). https://doi.org/10.1007/BF01323332

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01323332

Keywords

Navigation