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Morphological, biochemical and molecular changes during ectomycorrhiza development

  • Multi-Author Review
  • Structure, Function and Ecology of the Mycorrhizal Symbiosis
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“Puisant mes forces aux sources des galaxies En buvant la sève des arbres” M. Jonasz

Summary

An ectomycorrhiza, a specialized root organ, is the result of a complex interaction leading to a finely-tuned symbiosis between a plant and a compatible ectomycorrhizal fungus. Ultrastructural observations combined with cytochemical and biochemical studies reveal that structural and metabolic changes in the symbiont cells lead to the final phenotype of the active ectomycorrhiza. In the present review these changes are interpreted as changes in gene expression and discussed within the context of ectomycorrhiza development. Recent genetic data indicate that the continued vegetative growth of the ectomycorrhizal hyphae and the root tissues, and their ability to switch to symbiotic organ formation, is basically controlled by developmentally critical genes. The activity of these ‘symbiotic genes’ during the differentiation of ectomycorrhizas is associated with extensive changes in the concentration of particular polypeptides and protein biosynthesis. The present state of knowledge about the developmental biology of ectomycorrhizas allows only speculation about the events during their development.

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References

  1. Adams, T. H., Boylan, M. T., and Timberlake, W. E., brlA is necessary and sufficient to direct conidiophore development inAspergillus nidulans. Cell54 (1988) 353–362.

    Google Scholar 

  2. Al Abras, K., Bilger, I., Martin, F., Le Tacon, F., and Lapeyrie, F., Morphological and physiological changes in ectomycorrhizas of spruce (Picea excelsa (Lam.)Link) associated with ageing. New Phytol.110 (1988) 535–540.

    Google Scholar 

  3. Anderson, A. J., Mycorrhizae—Host specificity and recognition. Phytopathology78 (1988) 375–378.

    Google Scholar 

  4. Berlin, V., and Yanofski, C., Isolation and characterization of genes differentially expressed during conidiation ofNeurospora crassa. Molec. cell. Biol.5 (1985) 849–855.

    Google Scholar 

  5. Bilger, I., Guillot, V., Martin, F., and Le Tacon, F., Assessment of the contributions of glycolysis and the pentose phosphate pathway to glucose respiration in ectomycorrhizas and non-mycorrhizal roots of spruce (Picea abies L. Karsten). Ann. Sci. For.46 (1989) 794–797.

    Google Scholar 

  6. Bonfante-Fasolo, P., The role of the cell wall as a signal in mycorrhizal associations. NATO ISI SeriesH17 (1988) 219–235.

    Google Scholar 

  7. Botton, B., Chalot, M., and Dell, B., Changing electrophoretic patterns of glutamate dehydrogenases and aspartate aminotransferases in a few tree species under the influence of ectomycorrhization. Ann. Sci. For.46 (1989) 718–720.

    Google Scholar 

  8. Collinge, D. B., and Slusarenko, A. J., Plant gene expression in response to pathogens. Plant molec. Biol.9 (1987) 389–410.

    Google Scholar 

  9. Debaud, J. C., Gay, G., Prevost, A., Lei, J., and Dexheimer, J., Ectomycorrhizal ability of genetically different homokaryotic and dikaryotic mycelia ofHebeloma cylindrosporum. New Phytol.108 (1988) 323–328.

    Google Scholar 

  10. Dell, B., Botton, B., Martin, F., and Le Tacon, F., Glutamate dehydrogenases in ectomycorrhizas of spruce [Picea excelsa (Lam.)Link] and beech (Fagus sylvatica L.). New Phytol.111 (1989) 683–692.

    Google Scholar 

  11. Duc, G., Trouvelot, A., Gianinazzi-Pearson, V., and Gianinazzi, S., First report of nonmycorrhizal plant mutants (Myc-) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Sci.60 (1989) 215–222.

    Google Scholar 

  12. Flint, H. J., Changes in gene expression elicited by amino acid limitation inNeurospora crassa strains having normal or mutant cross-pathway amino acid control. Molec. gen. Genet.200 (1985) 283–290.

    Google Scholar 

  13. Frankenberger Jr, W. T., and Poth, M., Biosynthesis of indole-3-acetic acid by the pine ectomycorrhizal fungusPisolithus tinctorius. Appl. Environ. Microbiol.53 (1987) 2908–2913.

    Google Scholar 

  14. Fries, N., Ecological and evolutionary aspects of spore germination in the higher basidiomycetes. Trans. Br. mycol. Soc.88 (1987) 1–7.

    Google Scholar 

  15. Fries, N., Serck-Hanssen, K., Häll-Dimberg, L., and Theander, O., Abietic acid, an activator of basidiospore germination in ectomycorrhizal species of the genusSuillus (Boletaceae). Exp. Mycol.11 (1987) 360–363.

    Google Scholar 

  16. Gay, G., Rôle des hormones fongiques dans l'association ectomycorhizienne. Cryptogamie, Mycologie9 (1988) 211–220.

    Google Scholar 

  17. Gay, G., and Debaud, J. C., Genetic study on indole-3-acetic acid production by ectomycorrhizalHebeloma species: inter- and intraspecific variability in homo- and dikaryotic mycelia. Appl. Microbiol. Biotechnol.26 (1987) 141–146.

    Google Scholar 

  18. Gianinazzi-Pearson, V., Host-fungus specificity, recognition and compatibility in mycorrhizae, in: Plant Gene Research. Genes Involved in Microbe-Plant Interactions, pp. 225–253. Eds D. P. S. Verma and T. H. Höhn. Springer Verlag, New York 1988.

    Google Scholar 

  19. Goldstein, A. H., Mayfield, S. P., Danon, A., and Tibbot, B. K., Phosphate starvation inducible metabolism inLycopersicon esculentum. III. Changes in protein secretion under nutrient stress. Plant Physiol.91 (1989) 175–182.

    Google Scholar 

  20. Gooday, G. W., The hyphal tip, in: Fungal Differentiation. A Contemporary Synthesis, 9th edn, pp. 315–356. Ed. J. E. Smith. Marcel Dekker, New York 1986.

    Google Scholar 

  21. Gregory, P. H., The fungal mycelium: an historical perspective. Trans. Br. mycol. Soc.82 (1984) 1–11.

    Google Scholar 

  22. Grente, J., Chevalier, G., and Pollacsek, A., La germination de l'ascospore deTuber melanosporum et la synthèse sporale des mycorhizes. C. Acad. Sci.275 (1972) 743–746.

    Google Scholar 

  23. Guillot, J., Genaud, L., Geugnot, J., and Damez, M., Purification and properties of two hemagglutinins of the mushroomLaccaria amethystina. Biochem.22 (1983) 5365–5369.

    Google Scholar 

  24. Halverson, L. J., and Stacey, G., Signal exchange in plant-microbe interactions. Microbiol. Rev.50 (1986) 193–225.

    Google Scholar 

  25. Harley, J. L., and Smith, S. E., Mycorrhizal Symbiosis. Academic Press, London 1983.

    Google Scholar 

  26. Hernandez, G., Sanchez-Pescador, R., Palacios, R., and Mora, J., Nitrogen source regulates NADP-glutamate dehydrogenase synthesis inNeurospora crassa. J. Bact.154 (1983) 524–528.

    Google Scholar 

  27. Hilbert, J.-L., and Martin, F., Regulation of gene expression in ectomycorrhizas. I. Protein changes and the presence of ectomycorrhiza-specific polypeptides in thePisolithus-Eucalyptus symbiosis. New Phytol.110 (1988) 339–346.

    Google Scholar 

  28. Hilbert, J.-L., Costa, G., and Martin, F., Ectomycorrhizin synthesis and polypeptide changes during the early stages of eucalypt mycorrhiza development. Plant Physiol. (1991) in press.

  29. Horan, D. P., Chilvers, G. A., and Lapeyrie, F. F., Time sequence of the infection process in eucalypt ectomycorrhizas. New Phytol.109 (1988) 451–458.

    Google Scholar 

  30. Kottke, I., and Oberwinkler, F., Root-fungus interactions observed on initial stages of mantle formation and Hartig net establishment in mycorrhizas ofAmanita muscaria onPicea abies in pure culture. Can. J. Bot.64 (1986) 2348–2354.

    Google Scholar 

  31. Kottke, I., and Oberwinkler, F., The cellular structure of the Hartig net: coenocytic and transfer cell-like organization. Nord. J. Bot.7 (1987) 85–95.

    Google Scholar 

  32. Kottke, I., and Oberwinkler, F., Amplification of root-fungus-interface in ectomycorrhizae by Hartig net architecture. Ann. Sci. For.46 (1989) 737–740.

    Google Scholar 

  33. Kropp, B. R., and Fortin, J. A., The incompatibility system and relative ectomycorrhizal performance of monokaryons and reconstituted dikaryons ofLaccaria bicolor. Can. J. Bot.66 (1988) 289–294.

    Google Scholar 

  34. Kropp, B. R., McAfec, B. J., and Fortin, J. A., Variable loss of ectomycorrhizal ability in monokaryotic and dikaryotic cultures ofLaccaria bicolor. Can. J. Bot.65 (1986) 500–504.

    Google Scholar 

  35. Krupa, S., Fontana, A., and Palenzona, M., Studies on the nitrogen metabolism in ectomycorrhizae. I. Status of free and bound amino acids in mycorrhizal and nonmycorrhizal roots systems ofPinus nigra andCorylus avellana. Physiol. Plant.28 (1973) 1–6.

    Google Scholar 

  36. Krupa, S., and Branstrom, G., Studies on the nitrogen metabolism in ectomycorrhizae. II. Free and bound amino acids in the mycorrhizal fungusBoletus variegatus, in the root systems ofPinus sylvestris and during their association. Physiol. Plant.31 (1974) 279–283.

    Google Scholar 

  37. Lamhamedi, M. S., Fortin, A. J., Kope, H. H., and Kropp, B. R., Genetic variation in ectomycorrhiza formation byPisolithus tinctorius onPinus pinaster andPinus banksiana. New Phytol.115 (1990) 689–697.

    Google Scholar 

  38. Lapeyrie, F., Lei, J., Malajczuk, N., and Dexheimer, J., Ultrastructural and biochemical changes at the pre-infection stage of mycorrhizal formation by two isolates ofPisolithus tinctorius. Ann. Sci. For.46 (1989) 754–757.

    Google Scholar 

  39. Malajczuk, N., Lapeyrie, F., and Garbaye, J., Infectivity of pine and eucalypt isolates ofPisolithus tinctorius on roots ofEucalyptus urophylla in vitro. New Phytol.114 (1990) 627–631.

    Google Scholar 

  40. Marks, G. C., and Foster, R. C., Structure, morphogenesis and ultrastructure of ectomycorrhizae, in: Ectomycorrhizae, their Ecology and Physiology, pp. 1–40. Eds G. C. Marks and T. T. Kozlowski. Academic Press, New York 1973.

    Google Scholar 

  41. Marshall, J. D., and Perry, D. A., Basal and maintenance respiration of mycorrhizal and nonmycorrhizal root systems of conifers. Can. J. For. Res.17 (1987) 872–877.

    Google Scholar 

  42. Martin, F., Stewart, G. R., Genetet, I., and Le Tacon, F., Assimilation of 15 NH 4 + by beech (Fagus sylvatica L.) ectomycorrhizas. New Phytol.102 (1986) 85–94.

    Google Scholar 

  43. Martin, F., Ramstedt, M., and Söderhäll, K., Carbon and nitrogen metabolism in ectomycorrhizal fungi and ectomycorrhizas. Biochimie69 (1987) 569–581.

    Google Scholar 

  44. Massicotte, H. B., Ackerley, C. A., and Peterson, R. L., Localization of three sugar residues in the interface of ectomycorrhizae synthesized betweenAlnus crispa andAlpova diplophloeus as demonstrated by lectin binding. Can. J. Bot.65 (1987) 1127–1132.

    Google Scholar 

  45. Massicotte, H. B., Peterson, R. L., and Ashford, A. E., Ontogeny ofEucalyptus pilularis-Pisolithus tinctorius ectomycorrhizae. II. Transmission electron microscopy. Can. J. Bot.65 (1987) 1940–1947.

    Google Scholar 

  46. Massicotte, H. B., Peterson, R. L., and Melville, L. H., Ontogeny ofAlnus rubra-Alpova diplophoeus ectomycorrhizae. I. Light microscopy and scanning electron microscopy. Can. J. Bot.67 (1989) 191–200.

    Google Scholar 

  47. Mendgen, K., Schneider, A., Sterk, M., and Fink, W., The differentiation of infection structures as a result of recognition events between some biotrophic parasites and their hosts. J. Phytopath.123 (1988) 259–272.

    Google Scholar 

  48. Muramatsu, T., Alterations of cell-surface carbohydrates during differentiation and development. Biochimie70 (1988) 1587–1596.

    Google Scholar 

  49. Petit, P., Lallemant, R., and Savoye, D., Purified phytolectin from the lichenPeltigera canina var.canina which binds to the phycobiont cell walls and its use as cytochemical marker in situ. New Phytol.94 (1983) 103–110.

    Google Scholar 

  50. Piché, Y., Peterson, R. L., and Massicotte, H. B., Host-fungus interactions in ectomycorrhizae. Cell to cell signals in plant, animal and microbial symbiosis, vol. H17, 55–71. Eds Scannerini et al., NATO ISI, Series 1988.

  51. Pukkila, P. J., Binninger, D. M., Cassidy, J. R., Meiosis and genetic recombination inCoprinus cinereus, in: Developmental Biology of Higher Fungi, pp. 499–512. Eds D. Moore, L. A. Casselton, D. A. Wood and J. C. Frankland. Cambridge University Press, Cambridge 1985.

    Google Scholar 

  52. Ramstedt, M., Physiology of the ectomycorrhizal fungusPiloderma croceum, with emphasis on mannitol metabolism. Acta Univ. upsal., Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science 7, 1985.

  53. Raudaskoski, M., Sala, V., and Niini, S. S., Structure and function of the cytoskeleton in filamentous fungi.Karstenia 28 (1988) 49–60.

    Google Scholar 

  54. Rayner, A. D. M., Powell, K. A., Thompson, W., and Jennings, D. H., Morphogenesis of vegetative organs, in: Developmental Biology of Higher Fungi, pp. 249–280. Eds D. Moore, L. A. Casselton, D. A. Wood and J. C. Frankland. Cambridge University Press, Cambridge 1985.

    Google Scholar 

  55. Reijnders, A. F. M., and Moore, D., Developmental biology of agarics, in: Developmental Biology of Higher Fungi, pp. 581–595. Eds D. Moore, L. A. Casselton, D. A. Wood and J. C. Frankland. Cambridge University Press, Cambridge 1985.

    Google Scholar 

  56. Rouillon, R., Gay, G., Bernillon, J., Favre-Bonvin, J., and Bruchet, G., Analysis by HPLC-mass spectrometry of the indole compounds released by the ectomycorrhizal fungusHebeloma hiemale in pure culture. Can. J. Bot.64 (1986) 1893–1897.

    Google Scholar 

  57. Rupp, L. A., Mudge, K. W., and Negm, F. B., Involvement of ethylene in ectomycorrhiza formation and dichotomous branching of roots of mugo pine seedlings. Can. J. Bot.67 (1989) 477–482.

    Google Scholar 

  58. Smith, S. E., and Gianinazzi-Pearson, V., Physiological interactions between symbionts in vesicular arbuscular mycorrhizal plants. A. Rev. Plant Physiol.39 (1988) 221–244.

    Google Scholar 

  59. Smith, S. E., and Smith, F. A., Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol.114 (1990) 1–38.

    Google Scholar 

  60. Straker, C. J., Gianinazzi-Pearson, V., Gianinazzi, S., Cleyet-Marel, J. C., and Bousquet, N., Electrophoretic and immunological studies on acid phosphatase from a mycorrhizal fungus ofErica hispidula L. New Phytol.111 (1989) 215–221.

    Google Scholar 

  61. Verma, D. P. S., Fortin, M. G., Stanley, J., Mauro, V. P., Purohit, S., Morrison, N., Nodulins and nodulin genes ofGlycine max. Plant molec. Biol.7 (1986) 51–61.

    Google Scholar 

  62. Vézina, L. P., Margolis, H. A., McAfee, B. J., and Delaney, S., Changes in the activity of enzymes involved with primary nitrogen metabolism due to ectomycorrhizal symbiosis on jack pine seedlings. Physiol. Plant.75 (1989) 55–62.

    Google Scholar 

  63. Wessels, J. G. H., Gene expression during basidiocarp formation inSchizophyllum commune, in: Molecular Genetics of Filamentous Fungi, pp. 193–206. Ed W. E. Timberlake. Alan R. Liss, New York 1985.

    Google Scholar 

  64. Wong, K. K., Piché, Y., Montpetit, D., and Kropp, B. R., Differences in the colonization ofPinus banksiana roots by sib-monokaryotic and dikaryotic strains of ectomycorrhizalLaccaria bicolor. Can. J. Bot.67 (1989) 1717–1726.

    Google Scholar 

  65. Yoshida, K., Kuromitsu, Z., Ogawa, N., Ogawa, K., and Oshima, Y., Regulatory circuit for phosphatase synthesis inSaccharomyces cerevisiae, in: Phosphate Metabolism and Cellular Regulation in Microorganisms, pp. 49–55. Eds A. Torriani-Gorini, F. G. Rothman, S. Silver, A. Wright, and E. Yagil. American Society for Microbiology, Washington DC 1987.

    Google Scholar 

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  1. Laboratoire de Microbiologie Forestière, Centre de Recherches Forestières de Nancy, Institut National de la Recherche Agronomique, F-54280, Champenoux, France

    F. M. Martin & J. L. Hilbert

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Martin, F.M., Hilbert, J.L. Morphological, biochemical and molecular changes during ectomycorrhiza development. Experientia 47, 321–331 (1991). https://doi.org/10.1007/BF01972073

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