Plant and Soil

, Volume 159, Issue 1, pp 123–132 | Cite as

Interactions between mycorrhizal fungi and other soil organisms

  • A. H. Fitter
  • J. Garbaye
Article

Abstract

Mycorrhizal fungi interact with a wide range of other soil organisms, in the root, in the rhizosphere and in the bulk soil. These interactions may be inhibitory or stimulatory; some are clearly competitive, others may be mutualistic. Effects can be seen at all stages of the mycorrhizal fungal life-cycle, from spore population dynamics (predation, dispersal and germination) through root colonization to external hyphal growth. Two areas that seem likely to be of particular importance to the functioning of the symbiosis are the role of bacteria in promoting mycorrhiza formation and of soil animals in grazing the external mycelium. Mycorrhizal fungi also modify the interactions of plants with other soil organisms, both pathogens, such as root-inhabiting nematodes and fungi, and mutualists, notably nitrogen-fixing bacteria. These interactions are probably important both in natural ecosystems, where pathogens are increasingly recognized as playing controlling roles, and in agricultural systems, where mycorrhizas may be valuable in designing integrated systems of pest control and growth stimulation.

Key words

animals bacteria competition mutualism mycorrhizas pathogens soil organisms 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. AlexanderH M 1990 Dynamics of plant-pathogen interactions in natural plant communities. In Pests, Pathogens and Plant Communities. Eds. J JBurdon and S RLeather. pp 31–48. Blackwell Scientific Publications, Oxford, UK.Google Scholar
  2. AmesR N 1989 Mycorrhiza development in onion in response to inoculation with chitin-decomposing actinomycetes. New Phytol. 112, 423–427.CrossRefGoogle Scholar
  3. AsimiS, Gianinazzi-Pearson and GianinazziS 1980 Influence of increasing soil phosphorus level on interaction between vesicular-arbuscular mycorrhizae and Rhizobium in soybean. Can. J. Bot. 58, 2200–2205.Google Scholar
  4. Azcon-AguilarC, Diaz-RodriguezR M and BareaJ M 1986 Effect of soil microorganisms on spore germination of the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Trans. Br. Mycol. Soc. 86, 337–340.CrossRefGoogle Scholar
  5. BowenG D and TheodorouC 1979 Interactions between bacteria and ectomycorrhizal fungi. Soil Biol. Biochem. 11, 119–126.CrossRefGoogle Scholar
  6. BoyetchkoS M and TewariJ P 1991 Parasitism of spores of the vesicular-arbuscular mycorrhizal fungus Glomus dimorphicum. Phytoprotection 72, 27–32.Google Scholar
  7. CareyP D, FitterA H and WatkinsonA R 1992 A field study using the fungicide benomyl to investigate the effect of mycorrhizal fungi on plant fitness. Oecologia 90, 550–555.CrossRefGoogle Scholar
  8. CaronM 1989 Problematique de l'utilisation des champignons endomycorhiziens commeagents de lutte biologique. Phytoprotection 70, 43–49.Google Scholar
  9. CastellanoM A and TrappeJ M 1985 Ectomycorrhizal formation and plantation performance of Douglas-fir nursery stock inoculated with Rhizopogon spores. Can. J. For. Res. 15, 613–617.Google Scholar
  10. ChanwayC P, TurkingtonR and HollF B 1991 Ecological implications of specificity between plants and rhizosphere microorganisms. Adv. Ecol. Res. 21, 122–170.Google Scholar
  11. DuponnoisR and GarbayeJ 1991a Mycorrhization helper bacteria associated with the Douglas fir Laccaria laccata symbiosis: effects in vitro and in glasshouse conditions. Ann. Sci. For. 48, 239–251.Google Scholar
  12. DuponnoisR and GarbayeJ 1991b Some mechanisms involved in growth stimulation of ectomycorrhizal fungi by bacteria. Can. J. Bot. 68, 2148–2152.Google Scholar
  13. FinlayR D 1985 Interactions between soil micro-arthropods and endomycorrhizal associations of higher plants. In Ecological Interactions in Soil. Ed. A HFitter. pp 319–332. Blackwell Scientific Publications, Oxford, UK.Google Scholar
  14. FitterA H 1985 Functioning of vesicular-arbuscular mycorrhizas under field conditions. New Phytol. 99, 257–265.CrossRefGoogle Scholar
  15. FitterA H and NicholsR L 1988 The use of benomyl to control infection by vesicular-arbuscular mycorrhizal fungi. New Phytol. 109, 201–206.CrossRefGoogle Scholar
  16. FitterA H and SandersI R 1992 Interactions with the soil fauna. In Mycorrhizal Functioning. Ed. M FAllen. pp 333–354. Chapman and Hall, New York, USA.Google Scholar
  17. FogelR and TrappeJ M 1978 Fungus consumption (mycophagy) by small mammals. Northwest Sci. 52, 1–31.Google Scholar
  18. Fraga-BeddiarA and LeTaconF 1990 Interactions between VA mycorrhizal fungi and Frankia associated with alder (Alnus glutinosa). Symbiosis 9, 247–258.Google Scholar
  19. GarbayeJ 1991 Biological interactions in the mycorhizospere. Experientia 47, 370–375.CrossRefGoogle Scholar
  20. GarbayeJ and BowenG D 1987 Effect of different microflora on the success of ectomycorrhizal inoculation of Pinus radiata. Can. J. For. Res. 17, 941–943.Google Scholar
  21. GarbayeJ and BowenG D 1989 Stimulation of ectomycorrhizal infection of Pinus radiata by some microorganisms associated with the mantle of ectomycorrhizas. New Phytol. 112, 383–388.CrossRefGoogle Scholar
  22. Garbaye J and Duponnois R 1991 Specificity and function of mycorrhization helper bacteria (MHB) associated with the Pseudotsuga menziesii-Laccaria laccata symbiosis. Proc. International Symbiosis Congress, Jerusalem, Israel.Google Scholar
  23. Garcia GarridoJ M and OcampoJ A 1989 Effect of VA mycorrhizal infection of tomato on damage caused by Pseudomonas syringae. Soil Biol. Biochem. 21, 165–167.CrossRefGoogle Scholar
  24. GrahamJ H 1987 Non-nutritional benefits of VAM fungi. Do they exist? In Mycorrhizae in the Next Decade: Practical Applications and Research Priorities, Proc. 7th NACOM. Ed. D MSylvia, L LHung and J HGraham. pp 237–239. Institute of Food and Agricultural Sciences, University of Florida, Gainesville, Florida.Google Scholar
  25. GrahamJ H and LindermanR G 1980 Ethylene production by ectomycorrhizal fungi, Fusarium oxysporum f. sp. pini and by aseptically synthesized ectomycorrhizae and fusarium-infected Douglas-fir roots. Can. J. Microbiol. 26, 1340–1347.PubMedCrossRefGoogle Scholar
  26. HanlonR D G 1981 Influence of grazing by Collembola on the activity of senescent fungal colonies grown on media of different nutrient concentration. Oikos 36, 362–367.Google Scholar
  27. HarrisK K and BoernerR E J 1990 Effects of below ground grazing by Collembola on growth, mycorrhizal infection, and P uptake of Geranium robertianum. Plant Soil 129, 203–210.Google Scholar
  28. KaiserP A and LussenhopJ 1991 Collembolan effects on establishment of vesicular-arbuscular mycorrhizae in soybean (Glycine max). Soil Biol. Biochem. 23, 307–308.CrossRefGoogle Scholar
  29. Kellam M K and Schenck N C 1977 The effect of initial sequence on the interaction between Glomus macrocarpus and Meloidogyne incognita on soybean. In Proc. 3rd NACOM, Georgia, USA. p 3.Google Scholar
  30. KlyuchnikovA A and KozhevinP A 1990 Dynamics of Pseudomonas fluorescens and Azospirillum brasilense populations during the formation of the vesicular-arbuscular mycorrhiza. Microbiology 59, 449–452.Google Scholar
  31. KrupaS and FriesN 1971 Studies on ectomycorrhizae of pine. I—production of volatile organic compounds. Can. J. Bot. 49, 1425–1431.Google Scholar
  32. LindermanR G and PaulitzT C 1990 Mycorrhizal-rhizobacterial interactions. In Biological Control of Soil-borne Plant Pathogens. Ed. DHornby pp 261–283. Wallington, CAB International.Google Scholar
  33. McAfeeJ and FortinJ A 1988 Comparative effect of the soil microflora on ectomycorrhizal inoculation of conifer seedlings. New Phytol. 108, 443–449.CrossRefGoogle Scholar
  34. MalajczukN 1988 Interactions between Phytophthora cinnamomi zoospores and microorganisms on non-mycorrhizal and ectomycorrhizal roots of Eucalyptus marginata. Trans. Br. Mycol. Soc. 90, 375–382.CrossRefGoogle Scholar
  35. MamounM and OlivierJ M 1992 Effect of soil pseudomonads on colonization of hazel roots by the ectomycorrhizal species Tuber melanosporum and its competitors. Plant Soil 139, 265–273.CrossRefGoogle Scholar
  36. MarxD H 1969 The influence of ectotrophic mycorrhizae fungi of pine roots to pathogenic infection. II—Production, identification and biological activity of antibiotics produced by Leucopaxillus cerealis var. piceina. Phytopathology 59, 411–417.PubMedGoogle Scholar
  37. MarxD H 1972 Ectomycorrhizae as biological deterrents to pathogenic root infections. Ann. Revu. Phytopathol. 10, 429–454.CrossRefGoogle Scholar
  38. MayoK, DavisR and MottaJ 1986 Stimulation of germination of spores of Glomus versiforme by spore-associated bacteria. Mycologia 78, 426–431.Google Scholar
  39. MeyerJ R and LindermanR G 1986 Response of subterranean clover to dual inoculation with vesicular-arbuscular mycorrhizal fungi and a plant growth promoting rhizobacterium Pseudomonas putida. Soil Biol. Biochem. 18, 185–190.CrossRefGoogle Scholar
  40. MorandiD and BayletJ A 1984 Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiol. Plant Pathol. 24, 357–364.CrossRefGoogle Scholar
  41. MosseB 1962 The establishment of vesicular-arbuscular mycorrhiza under aseptic conditions. J. Gen. Microbiology 27, 509–520.Google Scholar
  42. MuchovejJ J, MuchovejR M C and GoncalvesE J 1991 Effect of kind and method of fungicidal treatment of bean seed on infections by the VA mycorrhizal fungus Glomus macrocarpum and by the pathogenic fungus Fusarium solani. 2. Temporal-spatial relationships. Plant Soil 132, 47–51.CrossRefGoogle Scholar
  43. O'BannonJ H and NemecS 1979 The response of Citrus limon seedlings to a symbiont, Glomus etunicatus and a pathogen, Radopholus similis. J. Nematol. 11, 270–275.PubMedGoogle Scholar
  44. PaulitzT C and MengeJ A 1984 Is Spizellomyces punctatum a parasite or a saprophyte of vesicular-arbuscular mycorrhizal fungi? Mycologia 76, 99–107.Google Scholar
  45. PaulitzT C and MengeJ A 1986 The effects of a mycoparasite on the mycorrhizal fungus Glomus deserticola. Phytopathology 76, 351–354.CrossRefGoogle Scholar
  46. PerrinR 1991 Mycorhizes et protection phytosanitaire. In Les mycorhizes des arbres etplantes cultives. Ed. StrulluD G. pp 93–130. Lavoisier, Paris, France.Google Scholar
  47. RabatinS C and StinnerB R 1988 Indirect effects of interactions between VAM fungi and soil-inhabiting in vertebrates on plant processes. Agric. Ecos. Env. 24, 135–146.CrossRefGoogle Scholar
  48. RidgeE H and TheodorouC 1972 The effect of soil fumigation on microbial recolonization and mycorrhizal infection. Soil Biol. Biochem. 4, 295–305.CrossRefGoogle Scholar
  49. RoncadoriR W and HusseyR S 1977 Interactions of the endomycorrhizal fungus Gigaspora margarita and root-knot nematode on cotton. Phytopathology 67, 1507.Google Scholar
  50. RossJ P and RuttencutterR 1977 Population dynamics of two vesicular-arbuscular endomycorrhizal fungi and the role of hyperparasitic fungi. Phytopathology 67, 490–496.Google Scholar
  51. SampangiR, PerrinR and LeTaconP 1986 Disease suppression and growth promotion of Norway spruce and Douglas-fir seedlings by the ectomycorrhizal fungus Laccaria laccata in forest nurseries. In Mycorrhizae: Physiology and Genetic. Ed. VGianinazzi. pp 799–806. Editions INRA, Paris, France.Google Scholar
  52. SchönbeckF 1979 Endomycorrhiza in relation to plant diseases. In Soil-borne Plant Pathogens. Eds. SchippersB and GamsW. pp 271–280. Academic Press, New York, USA.Google Scholar
  53. Sikora R A and Schönbeck F 1975 Effect of vesicular-arbuscular mycorrhiza (Endogone mosseae) on population dynamics of the root-knot nematodes (Meloidogyne incognita and M. hapla). VIII Int Congr. Plant Protect., Moscow. 5, 158.Google Scholar
  54. StrobelN E and SinclairW A 1991a Role of flavanolic wall infusions in the resistance induced by Laccaria bicolor to Fusarium oxysporum in primary roots of Douglas fir. Phytopathology 81, 420–425.Google Scholar
  55. StrobelN E and SinclairW A 1991b Influence of temperature and pathogen aggressiveness on biological control of Fusarium root rot by Laccaria bicolor in Douglas fir. Phytopathology 81, 415–420.Google Scholar
  56. SylviaD M and SchenckN C 1983 Soil fungicides for controlling chytridiaceous mycoparasites of Gigaspora margarita and Glomus fasciculatum. Appl. Environ. Microbiol. 45, 1306–1309.PubMedGoogle Scholar
  57. TothR, TothD, StarkeD and SmithD R 1990 vesicular-arbuscular mycorrhizal colonization in Zea mays affected by breeding for resistance to fungal pathogens. Can. J. Bot. 68, 1039–1044.Google Scholar
  58. TrofastJ and WickenbergB 1977 Mycorrhizin A and chloromycorrhizin A, two antibiotics from a mycorrhizal fungus of Monotropa hypopitys. Tetrahedron 33, 875–879.CrossRefGoogle Scholar
  59. TylkaG L, HusseyR S and RoncadoriR W 1991 Axenic germination of vesicular-arbuscular mycorrhizal fungi—effects of selected Streptomyces species. Phytopathology 81, 754–759.Google Scholar
  60. WarnockA J, FitterA H and UsherM B 1982 The influence of a springtail Folsomia candida (Insecta, Collembola) on the mycorrhizal association of leek Allium porrum and the vesicular-arbuscular mycorrhizal endophyte Glomus fasciculatus. New Phytol. 90, 285–292.CrossRefGoogle Scholar
  61. WilsonG W T, HetrickB A D and KittD G 1989 Suppression of vesicular-arbuscular mycorrhizal fungus spore germination by non-sterile soil. Can. J. Bot. 67, 18–23.Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • A. H. Fitter
    • 1
  • J. Garbaye
    • 2
  1. 1.Department of BiologyUniversity of YorkYorkUK
  2. 2.Laboratoire de Microbiologie ForestiereINRAChampenouxFrance

Personalised recommendations