Mycorrhiza pp 251-266 | Cite as

Proteins and Protein Activities in Endomycorrhizal Symbioses

  • V. Gianinazzi-Pearson
  • S. Gianinazzi


Virtually nothing is known of the molecular processes which determine the functional integration between symbionts in endomycorrhizal associations. The fact that, on the one hand, the obligate fungal biotrophs forming arbuscular endomycorrhizas (AM) cannot be maintained in pure culture without the host plant and that, on the other, ericoid or orchid endomycorrhizas have received relatively little attention, has retarded research advances in several domains, in particular those concerning fungal identification in planta, the molecular basis of compatible interactions, and the determination of functional symbioses in situ. However, some information has been obtained using approaches that are based on the metabolic activities of either symbiont in isolation or together. Proteins are key molecules in cellular metabolism and their most well-known physiological function is their role as enzymes. The aim of this presentation is not to give an exhaustive review on proteins and enzyme protein expression in endomycorrhizal symbionts (see Gianinazzi-Pearson and Smith 1993 for this), but rather to discuss what is known of their contribution to symbiont compatibility and their role as potential tools for identifying the fungal partner or the functional state of the symbiosis.


Fungal Symbiont Plasma Membrane ATPase Agric Ecosyst Environ Endomycorrhizal Fungus Periarbuscular Membrane 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abdel-Fattah GM (1991) Some ecological and physiological studies on vesicular-arbuscular (VA) mycorrhizal fungi. Thesis, Mansoura University, Egypt, 202 ppGoogle Scholar
  2. Barroso J, Pias MS (1990) Nuclear features in infected roots of Ophrys lutea Cay. ( Orchidaceae ). New Phytol 115: 93–98Google Scholar
  3. Berta G, Sgorbati S, Soler V, Fusconi A, Trotta A, Citterio A, Bottone MG, Sparvoli E, Scannerini S (1990) Variations in chromatin density in host nuclei of a vesicular arbuscular mycorrhiza. New Phytol 114: 199–205CrossRefGoogle Scholar
  4. Berta G, Sgorbati S, Giaccone P, Gianinazzi-Pearson V (1992) Nuclear morphology and ploidy level in infected and uninfected hair root cells of Calluna vulgaris and Vaccinium myrtillus mycorrhizae. Protoplasma 170: 160–165CrossRefGoogle Scholar
  5. Bonfante-Fasolo P, Gianinazzi-Pearson V (1982) Ultrastructural aspects of endomycorrhiza in the Ericaceae III Morphology of the dissociated symbionts and modifications occurring during their reassociation in axenic culture. New Phytol 91: 691–704CrossRefGoogle Scholar
  6. Bonfante-Fasolo P, Vian B, Perotto S, Faccio A, Knox JP (1990) Cellulose and pectin localization in roots of mycorrhizal Allium porrum: labelling continuity between host cell wall and interfacial material. Planta 180: 537–547CrossRefGoogle Scholar
  7. Bonfante-Fasolo P, Perotto S (1992) Plants and endomycorrhizal fungi: the cellular and molecular basis of their interaction. In: Verma DPS (ed) Molecular signals in plant-microbe interactions. CRC, Boca Raton, pp 445–470Google Scholar
  8. Capaccio LCM, Callow JA (1982) The enzymes of polyphosphate metabolism in vesicular-arbuscular mycorrhizas. New Phytol 91: 81–91CrossRefGoogle Scholar
  9. Cervone F, Castoria R, Spanu P, Bonfante-Fasolo P (1988) Pectinolytic activity in some ericoid mycorrhizal fungi. Trans Br Mycol Soc 91: 537–539CrossRefGoogle Scholar
  10. Daniels BA, Menge JA (1980) Hyperparasitization of vesicular-arbuscular mycorrhizal fungi. Phytopathology 70: 584–588CrossRefGoogle Scholar
  11. Dehne HW, Schönbeck F (1979) Untersuchungen zum Einfluss der endotrophen Mycorrhiza auf Pflanzenkrankheiten. 2. Phenolstoffwechsel und Lignifizierung. Phytopathol Z 95: 210–216Google Scholar
  12. Dehne HW, Schönbeck F, Baltruschat H (1978) Untersuchungen zum Einfluß der endotrophen Mykorrhiza auf Pflanzenkrankheiten. 3. Chitinase Aktivat und Ornithinzyklus. Z Pflanzenkr Pflanzenschutz 85: 666–678Google Scholar
  13. Dexheimer J, Gianinazzi S, Gianinazzi-Pearson V (1979) Ultrastructural cytochemistry of the host-fungus interfaces in the endomycorrhizal association Glomus mosseae/Allium cepa. Z Pflanzenphysiol 92: 191–206Google Scholar
  14. Dexheimer J, Gianinazzi-Pearson V, Gianinazzi S, Marx C (1982) Rôle possible de la vacuole du champignon symbiotique des mycorhizes VA dans la nutrition des plantes. Actual Bot 3: 29–34Google Scholar
  15. Dumas E, Gianinazzi-Pearson V, Gianinazzi S (1989) Production of new soluble proteins during VA endomycorrhiza formation. Agric Ecosyst Environ 29: 111–114CrossRefGoogle Scholar
  16. Dumas E, Tahiri-Alaoui A, Gianinazzi S, Gianinazzi-Pearson V (1990) Observations on modifications in gene expression with VA mycorrhiza development in tobacco: qualitative and quantitative changes in protein profiles. In: Nardon P, Gianinazzi-Pearson V, Grenier AM, Margulis L, Smith DC (eds) Endocytobiology IV. INRA, Paris, pp 153–157Google Scholar
  17. Dumas-Gaudot E, Furlan V, Grenier J, Asselin A (1992a) New acidic chitinase isoforms induced in tobacco roots by vesicular-arbuscular mycorrhizal fungi. Mycorrhiza 1: 133–136CrossRefGoogle Scholar
  18. Dumas-Gaudot E, Grenier J, Furlan V, Asselin A (1992b) Chitinase, chitosanase and ß-1,3-glucanase activities in Allium and Pisum roots colonized by Glomus species. Plant Sci 84: 17–24CrossRefGoogle Scholar
  19. Garcia-Garrido JM, Garcia-Romera I, Ocampo JA (1992) Cellulase production by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae (Nicol. and Gerd.) Gerd. and Trappe. New Phytol 121: 221–226Google Scholar
  20. Garcia-Garrido JM, Toro N, Ocampo JA (1993) Presence of specific polypeptides in onion roots colonized by Glomus mosseae. Mycorrhiza 2: 175–177CrossRefGoogle Scholar
  21. Garcia-Romera I, Garcia-Garrido JM, Ocampo JA (1991a) Pectolytic enzymes in the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. FEMS Microbiol Lett 78: 343–346CrossRefGoogle Scholar
  22. Garcia-Romera I, Garcia-Garrido JM, Ocampo JA (1991b) Pectinase activity in vesicular-arbuscular mycorrhiza during colonization of lettuce. Symbiosis 12: 189–198Google Scholar
  23. Gay JL (1984) Mechanisms of biotrophy in fungal pathogens. In: Wood RKS, Jellis GJ (eds) Plant diseases: infection, damage and loss. Blackwell, Oxford, pp 49–59Google Scholar
  24. Gehlert R, Kindl H (1991) Induced formation of dihydrophenanthrenes and bibenzyl synthase upon destruction of orchid mycorrhiza. Phytochemistry 30: 457–460CrossRefGoogle Scholar
  25. Gianinazzi S (1984) Genetic and molecular aspects of resistance induced by infection or chemicals. In: Nester T, Kosuge EW (eds) Plant microbe interactions, vol 1. Macmillan, New York, pp 321–342Google Scholar
  26. Gianinazzi S (1990) Vesicular-arbuscular (endo-) mycorrhizas: cellular, biochemical and genetic aspects. Agric Ecosyst Environ 35: 105–119CrossRefGoogle Scholar
  27. Gianinazzi S, Gianinazzi-Pearson V, Dexheimer J (1979) Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhiza III Ultrastructural localization of acid and alkaline phosphatase in onion roots infected by Glomus mosseae (Nicol. and Gerd. ). New Phytol 82: 127–132Google Scholar
  28. Gianinazzi S, Gianinazzi-Pearson V, Tisserant B, Lemoine MC (1992) Protein activities as potential markers of functional endomycorrhizas in plants. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Oxon, pp 333–339Google Scholar
  29. Gianinazzi-Pearson V (1984) Host-fungus specificity, recognition and compatibility in mycorrhizae. In: Verma DPS, Hohn T (eds) Genes involved in plant-microbe interactions. Plant gene research III. Springer, Vienna New York, pp 225–253CrossRefGoogle Scholar
  30. Gianinazzi-Pearson V, Gianinazzi S (1978) Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhiza II Soluble alkaline phosphatase specific to mycorrhizal infection in onion roots. Physiol Plant Pathol 12: 45–53CrossRefGoogle Scholar
  31. Gianinazzi-Pearson V, Gianinazzi S (1983) The physiology of vesicular-arbuscular mycorrhizal roots. Plant Soil 71: 197–209CrossRefGoogle Scholar
  32. Gianinazzi-Pearson V, Gianinazzi S (1989) Phosphorus metabolism in mycorrhizas. In: Boddy L, Marchant R, Read DJ (eds) Nitrogen, phosphorus and sulphur utilization by fungi. Cambridge University Press, Cambridge, pp 227–241Google Scholar
  33. Gianinazzi-Pearson V, Smith SE (1993) Physiology of mycorrhizal mycelia. Adv Plant Pathol 9: 55–82Google Scholar
  34. Gianinazzi-Pearson V, Gianinazzi S, Dexheimer J, Bertheau Y, Asimi S (1978) Les phosphatases alcalines solubles dans l’association endomycorhizienne à vésicules et arbuscules. Physiol Vég 16: 671–678Google Scholar
  35. Gianinazzi-Pearson V, Morandi D, Dexheimer J, Gianinazzi S (1981) Ultrastructural and ultracytochemical features of a Glomus tenuis mycorrhiza. New Phytol 88: 633–639CrossRefGoogle Scholar
  36. Gianinazzi-Pearson V, Dexheimer J, Gianinazzi S, Jeanmaire C (1984) Plasmalemma structure and function in endomycorrhizal symbioses. Z Pflanzenphysiol 114: 201–205Google Scholar
  37. Gianinazzi-Pearson V, Bonfante-Fasolo P, Dexheimer J (1986) Ultrastructural studies of surface interactions during adhesion and infection by ericoid endomycorrhizal fungi. NATO-ASI Ser H 4: 273–282Google Scholar
  38. Gianinazzi-Pearson V, Gianinazzi S, Brewin NJ (1990) Immunocytochemical localisation of antigenic sites in the perisymbiotic membrane of endomycorrhiza using monoclonal antibodies reacting against the peribacteroid membrane of nodules. In: Nardon P, Gianinazzi-Pearson V, Grenier AM, Margulis L, Smith DC (eds) Endocytobiology IV. INRA, Paris, pp 127–131Google Scholar
  39. Gianinazzi-Pearson V, Smith SE, Gianinazzi S, Smith FA (1991) Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas. V. Is H+ATPase a component of ATP-hydrolysing enzyme activities in plant-fungus interfaces? New Phytol 117: 61–74CrossRefGoogle Scholar
  40. Gianinazzi-Pearson V, Tahiri-Alaoui A, Antoniw JF, Gianinazzi S, Dumas-Gaudot E (1992) Weak expression of the pathogenesis-related PR-bl gene and localiza-tion of related protein during symbiotic endomycorrhizal interactions in tobacco roots. Endocytobiol Cell Res 8: 177–185Google Scholar
  41. Giovannetti M, Lioi L (1990) Variation of electrophoretic patterns in proteins of VAM fungi chlamydospores. Abstr 4th Int Mycological Congr, Regensburg, 323 ppGoogle Scholar
  42. Graham TL, Graham MY (1991) Cellular coordination of molecular responses in plant defense. Mol Plant-Microbe Interact 4: 415–422CrossRefGoogle Scholar
  43. Guillemin JP, Abdel-Fattah GM, Trouvelot A, Gianinazzi S, Gianinazzi-Pearson V (1993) Interactions between soil-applied fungicides, endomycorrhiza fungal activity and plant growth. Soil Sci Trends Agric Sci 1: 161–172Google Scholar
  44. Hepper CM, Sen R, Maskall CS (1986) Identification of vesicular-arbuscular mycorrhizal fungi in roots of leek ()Mum porrum L.) and maize (Zea mays L.) on the basis of enzyme mobility during polyacrylamide gel electrophoresis. New Phytol 102: 529–539CrossRefGoogle Scholar
  45. Hepper CM, Azcon-Aguilar C, Rosendahl S, Sen R (1988) Competition between three species of Glomus used as spatially separated introduced and indigenous inocula for leek ()Mum porrum L.). New Phytol 110: 207–215CrossRefGoogle Scholar
  46. Jacquelinet-Jeanmougin S, Gianinazzi-Pearson V, Gianinazzi S (1987) Endomycorrhizas in the Gentianaceae. II. Ultrastructural aspects of symbiont relationships in Gentiana lutea. Symbiosis 3: 269–286Google Scholar
  47. Jeanmaire C, Dexheimer J, Marx C, Gianinazzi S, Gianinazzi-Pearson V (1985) Effect of vesicular-arbuscular mycorrhizal infection on the distribution of neutral phosphatase activities in root cortical cells. J Plant Physiol 119: 285–293CrossRefGoogle Scholar
  48. Kough JL, Gianinazzi-Pearson V (1986) Physiological aspects of VA mycorrhizal hyphae in root tissue and soil. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 223–226Google Scholar
  49. Kough JL, Gianinazzi-Pearson V, Gianinazzi S (1987) Depressed metabolic activity of vesicular-arbuscular mycorrhizal fungi after fungicide application. New Phytol 106: 707–715CrossRefGoogle Scholar
  50. Lambais MR, Mehdy MC (1993) Suppression of endochitinase, 13–1,3-endoglucanase and chalcone isomerase expression in bean vesicular-arbuscular mycorrhizal roots under different soil phosphate conditions. Mol Plant-Microbe Interact 6: 75–83CrossRefGoogle Scholar
  51. Leake JR (1992) The role of ericoid mycorrhizas in the nitrogen nutrition and ecology of heathland systems. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Oxon, pp 227–236Google Scholar
  52. Lei J, Bécard G, Catford JG, Piché Y (1991) Root factors stimulate 32P uptake and plasmalemma ATPase activity in a vesicular-arbuscular fungus, Gigaspora margarita. New Phytol 118: 289–294CrossRefGoogle Scholar
  53. Lemoine MC, Gianinazzi-Pearson V, Gianinazzi S, Straker CJ (1992) Occurrence and expression of acid phosphatase of Hymenoscyphus ericae ( Read) Korf and Kernan, in isolation or in association with plant roots. Mycorrhiza 1: 137–146Google Scholar
  54. Marx C, Dexheimer J, Gianinazzi-Pearson V, Gianinazzi S (1982) Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhiza IV Ultracytoenzymological evidence ( ATPase) for active transfer processes in the host-arbuscule interface. New Phytol 90: 37–43Google Scholar
  55. McArthur DAJ, Knowles NR (1993) Influence of vesicular-arbuscular mycorrhizal fungi on the response of potato to phosphorus deficiency. Plant Physiol 101: 147–160PubMedGoogle Scholar
  56. Ocampo JA, Barea JM (1985) Effect of carbamate herbicides on VA mycorrhizal infection and plant growth. Plant Soil 85: 375–383CrossRefGoogle Scholar
  57. Ollivier B, Bertheau Y, Diem HG, Gianinazzi-Pearson V (1983) Influence de la variété de Vigna unguiculata dans l’expression de trois associations endomycorhizienns à vésicules et arbuscules. Can J Bot 61: 354–358CrossRefGoogle Scholar
  58. Pearson V, Read DJ (1975) The physiology of the mycorrhizal endophyte of Calluna vulgaris L. Hull. Trans Br Mycol Soc 64: 1–7Google Scholar
  59. Ravolanirina F (1990) L’endomycorhization VA des plantes ligneuses (vigne, pommier et poirier) micropropagées. Thesis, Dijon University, France, 131 ppGoogle Scholar
  60. Rosendahl S, Hepper CM (1987) Comparative studies of medium endophytes forming VA mycorrhizae. In: Sylvia DM, Hung LL, Graham JH (eds) Mycorrhizae in the next decade. Proc 7th NACOM, IFAS, University of Florida, 319 ppGoogle Scholar
  61. Rosendahl S, Sen R (1992) Isozyme analysis of mycorrhizal fungi and their mycorrhiza. Methods Microbiol 24: 169–194CrossRefGoogle Scholar
  62. Salomé M, Pais S, Barroso J (1983) Localization of polyphenoloxidases during the establishment of Ophrys lutea endomycorrhizas. New Phytol 95: 219–222CrossRefGoogle Scholar
  63. Sanders IR, Ravolanirina F, Gianinazzi-Pearson V, Gianinazzi S, Lemoine MC (1992) Detection of specific antigens in the vesicular-arbuscular mycorrhizal fungi Gigaspora margarita and Acaulospora laevis using polyclonal antibodies to soluble spore fractions. Mycol Res 96: 477–480CrossRefGoogle Scholar
  64. Schellenbaum L, Gianinazzi S, Gianinazzi-Pearson V (1992) Comparison of acid soluble protein synthesis in roots of endomycorrhizal wild type Pisum sativum and corresponding isogenic mutants. J Plant Physiol 141: 2–6CrossRefGoogle Scholar
  65. Schubert A, Marzachi C, Mazzitelli M, Cravero MC, Bonfante-Fasolo P (1987) Development of total and viable extraradical mycelium in the vesiculararbuscular mycorrhizal Glomus darum Nicol and Schenck. New Phytol 107: 183–190CrossRefGoogle Scholar
  66. Sen R, Hepper CM (1986) Characterization of vesicular-arbuscular mycorrhizal fungi (Glomus spp.) by selective enzyme staining following polyacrylamide gel electrophoresis. Soil Biol Biochem 18: 29–34CrossRefGoogle Scholar
  67. Serrano R (1990) Structure and function of plasma membrane ATPase. Annu Rev Plant Physiol Plant Mol Biol 40: 61–94CrossRefGoogle Scholar
  68. Serrigny J, Dexheimer J (1983) Etude ultrastructurale des endomycorhizes d’une orchidée tropicale Epidendrum ibaguense. II. Localisation des ATPases et des nucléosides diphosphatases. Cytologia 50: 779–788Google Scholar
  69. Serrigny J, Dexheimer J (1985) Endomycorhize d’une orchidée tropicale: Epidendrum ibaguense. Etude comparative des activités phosphatasiques acides entre le champignon associé et isolé. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 271–275Google Scholar
  70. Smith SE, Dickson S (1991) Quantification of active vesicular-arbuscular mycorrhizal infection using image analysis and other techniques. Aust J Plant Physiol 18: 637–648CrossRefGoogle Scholar
  71. Spanu P, Bonfante-Fasolo P (1988) Cell wall bound peroxidase activity in roots of mycorrhizal Allium porrum. New Phytol 109: 119–124CrossRefGoogle Scholar
  72. Spanu P, Boller T, Ludwig A, Wiemken A, Faccio A, Bonfante-Fasolo P (1989) Chitinase in roots of mycorrhizal Allium porrum: regulation and localization. Planta 177: 447–455CrossRefGoogle Scholar
  73. Spencer-Phillips PTN, Gay JL (1981) Domains of ATPase in plasma membranes and transport through infected plant cells. New Phytol 89: 393–400CrossRefGoogle Scholar
  74. Straker CJ, Mitchell DT (1986) The activity and characterisation of acid phosphatases in endomycorrhizal fungi of the Ericaceae. New Phytol 104: 243–256CrossRefGoogle Scholar
  75. Sylvia D (1988) Activity of external hyphae of vesicular-arbuscular mycorrhizal fungi. Soil Biol Biochem 20: 39–43CrossRefGoogle Scholar
  76. Tahiri-Alaoui A (1992) Modifications cellulaires et moléculaires après infection des racines de Nicotiana par le champignon pathogène Chalara elegans (Nag Rag and Ken.): mécanismes de defense et comparaison avec une infection symbiotique. Thesis, Dijon University, France, 189 ppGoogle Scholar
  77. Tahiri-Alaoui A, Dumas E, Gianinazzi S (1990) Detection of PR-b proteins in tobacco roots infected with Chalara elegans. Plant Mol Biol 14: 869–871PubMedCrossRefGoogle Scholar
  78. Tisserant B (1992) L’endomycorhization VA des ligneux: architecture racinaire et activité fonctionnelle de la symbiose endomycorhizienne. Thesis, Dijon University, France, 137 ppGoogle Scholar
  79. Tisserant B, Gianinazzi-Pearson V, Gianinazzi S, Gollotte A (1993) In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycol Res 97: 245–250CrossRefGoogle Scholar
  80. Vierheilig H, Ocampo JA (1989) Relationship between SDH-activity and VAmycorrhizal infection. Agric Ecosyst Environ 29: 439–442CrossRefGoogle Scholar
  81. Ward EWB (1986) Biochemical mechanisms involved in resistance of plants to fungi. NATO ASI Ser Cell Biol H1: 107–131Google Scholar
  82. Williamson B (1973) Acid phosphatase and esterase activity in orchid mycorrhiza. Planta 112: 149–158CrossRefGoogle Scholar
  83. Woods AM, Gay JL (1987) The interface between haustoria of Puccinia poarum (monokaryon) and Tussilago farfara. Physiol Mol Plant Pathol 30: 73–88CrossRefGoogle Scholar
  84. Wright SF, Morton JB (1989) Detection of vesicular-arbuscular mycorrhizal fungus colonization of roots using a dot-immunoblot assay. Appl Environ Microbiol 55: 761–763PubMedGoogle Scholar
  85. Wright SF, Morton JB, Sworobuk JE (1987) Identification of a vesicular-arbuscular mycorrhizal fungus by using monoclonal antibodies in an enzyme-linked immunoassay. Appl Environ Microbiol 52: 2222–2225Google Scholar
  86. Wyss P, Mellor RB, Wiemken A (1990) Vesicular-arbuscular mycorrhizas of wild-type soybean and non-nodulating mutants with Glomus mosseae contain symbiosis-specific polypeptides (mycorrhizins), immunologically cross-reactive with nodulins. Planta 182: 22–26CrossRefGoogle Scholar
  87. Added in proof. The reference list stops in autumn 1993 and since only limited opportunity for revision was given, the authors regret that this has inevitably resulted in omissions of more recent work.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1995

Authors and Affiliations

  • V. Gianinazzi-Pearson
  • S. Gianinazzi
    • 1
  1. 1.Laboratoire de PhytoparasitologieINRA-CNRS, Station de Génétique et d’Amélioration des PlantesDijon CédexFrance

Personalised recommendations