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Biocontrol of Soil Phytopathogens by Arbuscular Mycorrhiza – A Review

  • Pranay Jain
  • Ram Kumar Pundir
Chapter

Abstract

The symbiotic association of plants with fungus exhibited arbuscular mycorrhizal (AM) association that favour mineral and water nutrition and decrease abiotic and biotic stresses. It has been reported that approximately 90% of plants are colonized by the mycorrhizal fungi species ranging from angiosperms to gymnospermic plants, while several of them are devoid of AM fungi. During its life cycle, the arbuscular mycorrhizal fungi must have a host and this symbiotic association is reciprocally benign, where the AM provides help to the plant in nutrients uptake, and in return, the plant provides the fungus with carbon. The AM fungi have been used as a biocontrol agent in lieu of their antagonistic interaction with various soilborne plant pathogens. The review highlights various examples of use of AMF for the control of phytopathogenic flora and fauna. The present chapter reflects inclusive compilation that highlights the mechanisms adapted by AM Fungi for the control of pathogenic flora and fauna.

Keywords

Arbuscular mycorrhizal fungi Symbiosis Antagonistic interactions Biocontrol 

Notes

Acknowledgement

The authors are grateful to the Director, University Institute of Engineering and Technology, Kurukshetra University, Kurukshetra (Haryana, India) and Management of Ambala College of Engineering and Applied Research, Ambala (Haryana, India), for providing necessary infrastructure to carry out literature search.

References

  1. Alban, R., Guerrero, R., & Toro, M. (2013). Interactions between a root knot nematode (Meloidogyne exigua) and arbuscular mycorrhizae in coffee plant development (Coffea arabica). American Journal of Plant Sciences, 4, 19–23.CrossRefGoogle Scholar
  2. Augé, R. M. (2001). Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza, 11, 3–42.CrossRefGoogle Scholar
  3. Azcon-Aguilar, C., & Barea, J. M. (1992). Interactions between mycorrhizal fungi and other rhizosphere microorganisms. In M. F. Allen (Ed.), Mycorrhizal functioning: An integrative plant-fungal process (pp. 163–198). New York: Chapman and Hall.Google Scholar
  4. Azcon-Aguilar, C., Jaizme-Vega, M. C., & Calvet, C. (2002). The contribution of arbuscular mycorrhizal fungi for bioremediation. In S. Gianinazzi, H. Schuepp, J. M. Barea, & K. Haselwandter (Eds.), Mycorrhizal technology in agriculture. From genes to bioproducts (pp. 187–197). Berlin: Birkhauser Verlag.CrossRefGoogle Scholar
  5. Bago, B., Azcón-Aguilar, C., Goulet, A., & Piché, Y. (1998). Branched adsorbing structure (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi. The New Phytologist, 139, 375–388.CrossRefGoogle Scholar
  6. Bagyaraj, D. J. (1984). Biological interactions with VA mycorrhizal fungi. In C. L. Powell & D. J. Bagyaraj (Eds.), VA Mycorrhiza (pp. 131–153). Florida: CRC Press.Google Scholar
  7. Bansal, M., & Mukerji, K. G. (1996). Root exudates and its rhizosphere biology. In K. G. Mukerji, V. P. Singh, & S. Dwivedi (Eds.), Concepts in applied microbiology and biotechnology (pp. 79–119). New Delhi: Aditya Books Pvt Ltd.Google Scholar
  8. Barea, J. M., Pozo, M. J., Azcón, R., & Azcón-Aguilar, C. (2013). Microbial interactions in the rhizosphere. In F. de Bruijn (Ed.), Molecular microbial ecology of the rhizosphere (pp. 29–44). Hoboken: Wiley-Blackwell.CrossRefGoogle Scholar
  9. Baum, C., El-Tohamy, W., & Gruda, N. (2015). Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: A review. Scientia Horticculturae (Amsterdam), 187, 131–141.CrossRefGoogle Scholar
  10. Bever, J. D., Morton, J. B., Antonovics, J., & Schultz, P. A. (1996). Host dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. Journal of Ecology, 84, 71–82.CrossRefGoogle Scholar
  11. Bodker, L., Kjoller, R., & Rosendahl, S. (1998). Effect of phosphate and the arbuscular mycorrhizal fungus Glomus intraradices on disease severity of root rot of peas (Pisum sativum) caused by Aphanomyces euteiches. Mycorrhiza, 8, 169–174.CrossRefGoogle Scholar
  12. Bodker, L., Kjoller, R., Kristensen, K., & Rosendahl, S. (2002). Interactions between indigenous arbuscular mycorrhizal fungi and Aphanomyces euteiches in field-grown pea. Mycorrhiza, 12, 7–12.PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bonfante, P., & Desirò, A. (2015). Arbuscular mycorrhizas: The lives of beneficial fungi and their plant host. In B. Lugtenberg (Ed.), Principles of plant-microbe interactions (pp. 235–245). Cham: Springer.Google Scholar
  14. Boyetchko, S. M. (1996). Impact of soil microorganisms on weed biology and ecology. Phytoprotection, 77, 41–56.CrossRefGoogle Scholar
  15. Braga, M. R., et al. (1991). Phytoalexins induction in Rubiacea. Journal of Chemical Ecology, 17, 1079–1090.PubMedCrossRefPubMedCentralGoogle Scholar
  16. Brendan, N. A., Hammerschmidt, R., & Safir, G. R. (1996). Postharvest suppression of potato dry rot (Fusarium sambucinum) in prenuclear minitubers by arbuscular mycorrhizal fungal inoculum. American Potato Journal, 73, 509–515.CrossRefGoogle Scholar
  17. Brundrett, M. C. (2009). Mycorrhizal associations and other means of nutrition of vascular plants: Understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil, 320, 37–77.CrossRefGoogle Scholar
  18. Budi, S. W., van Tuinen, D., Martinotti, G., & Gianinazzi, S. (1999). Isolation from the Sorghum bicolor mycorrhizosphere of a bacterium compatible with arbuscular mycorrhiza development and antagonistic towards soilborne fungal pathogens. Applied and Environmental Microbiology, 65, 5148–5150.PubMedPubMedCentralGoogle Scholar
  19. Caron, M. (1989). Potential use of mycorrhizae in control of soil-borne diseases. Canadian Journal of Plant Pathology, 11, 177–179.CrossRefGoogle Scholar
  20. Caron, M., Fortin, J. A., & Richard, C. (1985). Influence of substrate on the interaction of Glomus intraradices and Fusarium oxysporum f. sp. radicis-lycopersici on tomatoes. Plant and Soil, 87, 233–239.CrossRefGoogle Scholar
  21. Caron, M., Fortin, J. A., & Richard, C. (1986). Effect of phosphorus concentration and Glomus intraradices on Fusarium crown and root rot of tomatoes. Phytopathology, 76, 942–946.CrossRefGoogle Scholar
  22. Cordier, C., Gianinazzi, S., & Gianinazzi-Pearson, V. (1996). Colonisation patterns of root tissues by Phytophthora nicotianae var. parasitica related to reduced disease in mycorrhizal tomato. Plant and Soil, 185, 223–232.CrossRefGoogle Scholar
  23. Cordier, C., Pozo, M. J., Barea, J. M., Gianiniazzi, S., & Gianinazzi-Pearson, V. (1998). Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Molecular Plant Microbe Interactions, 11, 1017–1028.CrossRefGoogle Scholar
  24. Dehne, H. W., & Schonbeck, F. (1979). The influence of endotrophic mycorrhiza on plant diseases. II. Phenol metabolism and lignification Fusarium oxysporum. Untersuchungen zum Einfluss der endotrophen Mycorrhiza auf Pflanzenkrankheiten. II. Phenolstoffwechsel und Lignifizierung. Phytopathologische Zeitschrift, 95, 210–216.CrossRefGoogle Scholar
  25. Druzhinina, I. S., Seidl-Seiboth, V., Herrera-Estrella, A., Horwitz, B. A., Kenerley, C. M., Monte, E., et al. (2011). Trichoderma: The genomics of opportunistic success. Nature Reviews Microbiology, 9, 749–759.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Elsen, A., Baimey, H., Swennen, R., & DeWaele, D. (2003). Relative mycorrhizal dependency and mycorrhiza nematode interaction in banana cultivars (Mus spp.) differing in nematode susceptibility. Plant and Soil, 256, 303–313.CrossRefGoogle Scholar
  27. Feldmann, F., & Boyle, C. (1998). Concurrent development of arbuscular mycorrhizal colonization and powdery mildew infection on three Begonia hiemalis cultivars. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz, 105, 121–129.Google Scholar
  28. Ferraz, L., & Brown, D. (2002). An introduction to nematodes—plant nematology. Sofia: Pensoft.Google Scholar
  29. Filion, M., St. Arnaud, M., & Fortin, J. A. (1999). Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. The New Phytologist, 141, 525–533.CrossRefGoogle Scholar
  30. Fitter, A. H., & Sanders, I. R. (1992). Interactions with the soil fauna. In M. F. Allen (Ed.), Mycorrhizal functioning: An integrative plant- fungal process (pp. 333–354). New York: Chapman and Hall.Google Scholar
  31. Frankenberger, W. T., & Arshad, M. (1995). Microbial biosynthesis of auxins. In W. T. Frankenberger & M. Arshad (Eds.), Phytohormones in soil (pp. 35–71). New York: Marcel Dekker.Google Scholar
  32. Frey-Klett, P., & Garbaye, J. (2005). Mycorrhiza helper bacteria: a promising model for the genomic analysis of fungal–bacterial interactions. The New Phytologist, 168, 4–8.PubMedCrossRefPubMedCentralGoogle Scholar
  33. Fritz, M., Jakobsen, I., Lyngkjaer, M. F., Thordal-Christensen, H., & Pons- Kühnemann, J. (2006). Arbuscular mycorrhiza reduces susceptibility of tomatoto Alternaria solani. Mycorrhiza, 16, 413–419.PubMedCrossRefPubMedCentralGoogle Scholar
  34. Garbaye, J. (1994). Tansley review No. 76 Helper bacteria: A new dimension to the mycorrhizal symbiosis. The New Phytologist, 128, 197–210.CrossRefGoogle Scholar
  35. Gheysen, G., & Mitchum, M. G. (2011). How nematodes manipulate plant development pathways for infection. Current Opinion in Plant Biology, 14, 415–421.PubMedCrossRefPubMedCentralGoogle Scholar
  36. Gianinazzi, S., & Schuepp, H. (1994). Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems (p. 226). Basel: Birkhauser Verlag.CrossRefGoogle Scholar
  37. Gianinazzi, S., Gollotte, A., Binet, M.-N., van Tuinen, D., Redecker, D., & Wipf, D. (2010). Agroecology: The key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza, 20, 519–530.PubMedCrossRefGoogle Scholar
  38. Graham, T. L., & Graham, M. Y. (1991). Cellular coordination of molecular responses in plant defense. Molecular Plant-Microbe Interactions, 4, 415–422.CrossRefGoogle Scholar
  39. Graham, J. H., Leonard, R. T., & Menge, J. A. (1981). Membrane mediated decrease in root exudation responsible for inhibition of vesicular-arbuscular mycorrhiza formation. Plant Physiology, 68, 548–552.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Grayston, S. J., Vaughan, D., & Jones, D. (1997). Rhizosphere carbon flow in trees, in comparison with annual plants: The importance of root exudation and its impact on microbial activity and nutrient availability. Applied Soil Ecology, 5, 29–56.CrossRefGoogle Scholar
  41. Gutjahr, C., & Parniske, M. (2013). Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annual Review of Cell and Developmental Biology, 29, 593–617.PubMedCrossRefPubMedCentralGoogle Scholar
  42. Gutjahr, C., & Paszkowski, U. (2013). Multiple control levels of root system remodeling in arbuscular mycorrhizal symbiosis. Frontiers in Plant Science, 4, 204.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hage-Ahmed, K., Moyses, A., Voglgruber, A., Hadacek, F., & Steinkellner, S. (2013). Alterations in root exudation of intercropped tomato mediated by the arbuscular mycorrhizal fungus Glomus mosseae and the soil borne pathogen Fusarium oxysporum f. sp. lycopersici. Journal of Phytopathology, 161, 763–773.CrossRefGoogle Scholar
  44. Hammer, E. C., Pallon, J., Wallander, H., & Olsson, P. A. (2011). Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiology Ecology, 76, 236–244.PubMedCrossRefPubMedCentralGoogle Scholar
  45. Handelsman, J., & Stabb, E. V. (1996). Biocontrol of soilborne plant pathogens. Plant Cell, 8, 1855–1869.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hao, Z., Fayolle, L., Van Tuinen, D., Chatagnier, O., Li, X., & Gianinazzi, S. (2012). Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defence gene responses in grapevine. Journal of Experimental Botany, 63, 3657–3672.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Harrier, L. A. (2001). The arbuscular mycorrhizal symbiosis: A molecular review of the fungal dimension. The Journal of Experimental Medicine, 52, 469–478.Google Scholar
  48. Harrier, L. A., & Watson, C. A. (2004). The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic and/or other sustainable farming systems (Special issue: Current research at the Scottish Agricultural College). Pest Management Science, 60, 149–157.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Hodge, A., Campbell, C. D., & Fitter, A. H. (2001). An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic matter. Nature, 413, 297–299.PubMedCrossRefPubMedCentralGoogle Scholar
  50. Hwang, S. F. (1988). Effect of VA mycorrhizae and metalaxyl on growth of alfalfa seedlings in soils from fields with “alfalfa sickness” in Alberta. Plant Disease, 72, 448–452.CrossRefGoogle Scholar
  51. Jabaji-Hare, S. H., & Stobbs, L. W. (1984). Electron microscopic examination of tomato roots coinfected with Glomus sp. and tobacco mosaic virus. Phytopathology, 74, 277–279.CrossRefGoogle Scholar
  52. Jaizme-Vega, M. C., Sosa-Hernandez, B., Hernandez, J. M., & Galan- Sauco, V. (1998). Interaction of arbuscular mycorrhizal fungi and the soil pathogen Fusarium oxysporum f. sp. cubense on the first stages of micropropagated Grande Naine banana. Acta Horticulturae, 490, 285–295.CrossRefGoogle Scholar
  53. Jansa, J., Mozafar, A., & Frossard, E. (2003). Long distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie, 23, 481–488.CrossRefGoogle Scholar
  54. Jeffries, P., & Barea, J. M. (2012). Arbuscular mycorrhiza-a key component of sustainable plant-soil ecosystems. In B. Hock (Ed.), The mycota (pp. 51–75). Berlin/Heidelberg: Springer.Google Scholar
  55. Jeffries, P., Gianinazzi, S., Perotto, S., Turnau, K., & Barea, J. M. (2003). The contribution of arbuscular mycorrhizal fungí in sustainable maintenance of plant health and soil fertility. Biology and Fertility of Soils, 37, 1–16.Google Scholar
  56. Johnson, N. C., Copeland, P. J., Crookston, R. K., & Pfleger, F. L. (1992). Mycorrhizae: Possible explanation for yield decline with continuous corn and soybean. Agronomy Journal, 84, 387–390.CrossRefGoogle Scholar
  57. Johnson, D., Leake, J. R., Ostle, N., Ineson, P., & Read, D. J. (2002a). In situ (CO2)–C-13 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytologist, 153, 327–334.CrossRefGoogle Scholar
  58. Johnson, D., Leake, J. R., & Read, D. J. (2002b). Transfer of recent photosynthate into mycorrhizal mycelium of an upland grassland: Short-term respiratory losses and accumulation of 14C. Soil Biology and Biochemistry, 34, 1521–1524.CrossRefGoogle Scholar
  59. Jones, J. D. G., & Dangl, J. L. (2006). The plant immune system. Nature, 444, 323–329.PubMedCrossRefPubMedCentralGoogle Scholar
  60. Jones, D. L., Hodge, A., & Kuzyakov, Y. (2004). Plant and mycorrhizal regulation of rhizo deposition. The New Phytologist, 163, 459–480.CrossRefGoogle Scholar
  61. Jones, J. T., Haegeman, A., Danchin, E. G. J., Gaur, H. S., Helder, J., MGK, J., et al. (2013). Top10plant-parasiticnematodesinmolecularplantpathology. Molecular Plant Pathology, 14, 946–961.PubMedCrossRefPubMedCentralGoogle Scholar
  62. Jung, S. C., Martinez-Medina, A., Lopez-Raez, J. A., & Pozo, M. J. (2012). Mycorrhiza-induced resistance and priming of plant defenses. Journal of Chemical Ecology, 38, 651–664.PubMedCrossRefPubMedCentralGoogle Scholar
  63. Khan, A. G., Kuek, C., Chaudhry, T. M., Khoo, C. S., & Hayes, W. J. (2000). Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere, 41, 197–207.PubMedPubMedCentralCrossRefGoogle Scholar
  64. Kobra, N., Jalil, K., & Youbert, G. (2009). Effects of three Glomus species as biocontrol agents against Verticillium-induced wilt in cotton. Journal of Plant Protection Research, 49, 185–189.CrossRefGoogle Scholar
  65. Kulkarni, S. A., Kulkarni, S., Sreenivas, M. N., & Kulkarni, S. (1997). Interaction between vesicular-arbuscular (VA) mycorrhizae and Sclerotium rolfsii Sacc. in groundnut. Karnataka Journal of Agricultural Science, 10, 919–921.Google Scholar
  66. Lambais, M. R., & Mehdy, M. C. (1995). Differential expression of defense-related genes in arbuscular mycorrhiza. Canadian Journal of Botany, 73, S533–S540.CrossRefGoogle Scholar
  67. Lerat, S., Lapointe, L., Piché, Y., & Vierheilig, H. (2003). Strains colonizing barley roots. Canadian Journal of Botany, 81, 886–889.CrossRefGoogle Scholar
  68. Li, S. L., Zhao, S. J., Zhao, L. Z., Li, S. L., Zhao, S. J., & Zhao, L. Z. (1997). Effects of VA mycorrhizae on the growth of eggplant and cucumber and control of diseases. Acta Phytophylacica Sinica, 24, 117–120.Google Scholar
  69. Linderman, R. G. (1988). Mycorrhizal interactions with the rhizosphere microflora-The Mycorrhizosphere effect. Proceedings of the American Phytopathology Society, 78(3), 366–371.Google Scholar
  70. Linderman, R. G. (1994). Role of VAM fungi in biocontrol. In F. L. Pfleger & R. G. Linderman (Eds.), Mycorrhizae and plant health (pp. 1–27). St. Paul: The American Phytopathological Society.Google Scholar
  71. Lioussanne, L., Jolicoeur, M., & St-Arnaud, M. (2008). Mycorrhizal colonization with Glomus intraradices and development stage of transformed tomato roots significantly modify the chemotactic response of zoospores of the pathogen Phytophthora nicotianae. Soil Biology and Biochemistry, 40, 2217–2224.CrossRefGoogle Scholar
  72. López-Ráez, J. A., Charnikhova, T., Fernández, I., Bouwmeester, H., & Pozo, M. J. (2011a). Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. Journal of Plant Physiology, 168, 294–297.PubMedCrossRefPubMedCentralGoogle Scholar
  73. López-Ráez, J. A., Pozo, M. J., & García-Garrido, J. M. (2011b). Strigolactones: A cry for help in the rhizosphere. Botany, 89, 513–522.CrossRefGoogle Scholar
  74. Maillet, F., Poinsot, V., André, O., Puech-Pagés, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., FormeyD, N. A., Martinez, E. A., Driguez, H., Bécard, G., & Dénarié, J. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature, 469, 58–64.PubMedCrossRefPubMedCentralGoogle Scholar
  75. McArthur, D. A., & Knowles, N. R. (1992). Resistance responses of potato to vesicular-arbuscular mycorrhizal fungi under varying abiotic phosphorus levels. Plant Physiology, 100, 341–351.PubMedPubMedCentralCrossRefGoogle Scholar
  76. McGonigle, T. P., & Miller, M. H. (1993). Mycorrhizal development and phosphorus absorption in maize under conventional and reduced tillage. Soil Science Society of America Journal, 57, 1002–1006.CrossRefGoogle Scholar
  77. McGonigle, T. P., & Miller, M. H. (1996). Mycorrhizae, phosphorus absorption, and yield of maize in response to tillage. Soil Science Society of America Journal, 60, 1856–1861.CrossRefGoogle Scholar
  78. Minerdi, D., Fani, R., Gallo, R., Boarino, A., & Bonfante, P. (2001). Nitrogen fixation genes in an endosymbiotic Burkholderia strain. Applied and Environmental Microbiology, 67, 725–732.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Morandi, D. (1996). Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control. Plant and Soil, 185, 241–251.CrossRefGoogle Scholar
  80. Mukerji, K. G., Manoharachary, C., & Chamola, B. P. (2002). Techniques in mycorrhizal studies (1st ed., pp. 285–296). London/Dordrecht: Kluwer Academic Publishers.CrossRefGoogle Scholar
  81. Nemec, S. (1994). Soil microflora associated with pot cultures of Glomus intraradix-infected Citrus reticulata. Agriculture, Ecosystems and Environment, 1, 299–306.Google Scholar
  82. Nemec, S., & Myhre, D. (1984). Virus–Glomus etunicatum interactions in citrus rootstocks [Sour orange, Citrus macrophylla, Duncan grapefruit, potential of mycorrhizal citrus rootstock seedlings to protect against growth suppression by viruses]. Journal of Plant Disease, 68, 311–314.CrossRefGoogle Scholar
  83. Newsham, K. K., Fitter, A. H., & Watkinson, A. R. (1995). Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. Journal of Ecology, 83, 991–1000.CrossRefGoogle Scholar
  84. Nicol, J. M., Turner, S. J., Coyne, D. L., den Nijs, L., Hockland, S., & Tahna Maafi, Z. (2011). Current nematode threats to world agriculture. In J. Jones, G. Gheysen, & C. Fenoll (Eds.), Genomics and molecular genetics of plant-Nematode interactions (pp. 347–367). Heidelberg: Springer.Google Scholar
  85. Norman, J., Atkinson, D., & Hooker, J. (1996). Arbuscular mycorrhizal fungal- induced alteration to root Architecture in strawberry and induced resistance to the root pathogen Phytophthora fragariae. Plant and Soil, 185, 191–198.CrossRefGoogle Scholar
  86. Nuccio, E. E., Hodge, A., Pett-Ridge, J., Herman, D. J., Weber, P. K., & Firestone, M. K. (2013). An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environmental Microbiology, 15, 1870–1881.PubMedCrossRefPubMedCentralGoogle Scholar
  87. Otto, G., & Winkler, H. (1995). Colonization of rootlets of some species of Rosaceae by actinomycetes, endotrophic mycorrhiza, and endophytic nematodes in a soil conducive to specific cherry replant disease. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz, 102, 63–68.Google Scholar
  88. Paulitz, T. C., & Linderman, R. G. (1989). Interactions between fluorescent pseudomonads and VA mycorrhizal fungi. The New Phytologist, 113, 37–45.CrossRefGoogle Scholar
  89. Paxton, J. D. (1981). Phytoalexins- A working redefinition. Journal of Phytopathology, 101(2), 106–109.CrossRefGoogle Scholar
  90. Perry, R. N., & Moens, M. (2011). Introduction to plant-parasitic nematodes; modes of parasitism. In T. Jones, L. Gheysen, & C. Fenoll (Eds.), Genomics and molecular genetics of plant–nematode interactions (pp. 3–20). Heidelberg: Springer.CrossRefGoogle Scholar
  91. Peterson, R. L., Massicotte, H. B., & Melville, L. H. (2004). Mycorrhizas: Anatomy and cell biology. Ottawa: NRC Research Press.Google Scholar
  92. Philippot, L., Raaijmakers, J. M., Lemanceau, P., & van der Putten, W. H. (2013). Going back to the roots: The microbial ecology of the rhizosphere. Nature Reviews. Microbiology, 11, 789–799.PubMedCrossRefPubMedCentralGoogle Scholar
  93. Pozo, M. J., & Azcón-Aguilar, C. (2007). Unraveling mycorrhiza-induced resistance. Current Opinion in Plant Biology, 10, 393–398.PubMedCrossRefPubMedCentralGoogle Scholar
  94. Pozo, M. J., Azcon-Aguilar, C., Dumas-Gaudot, E., & Barea, J. M. (1999). β-1,3-glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Science, 141, 149–157.CrossRefGoogle Scholar
  95. Pozo, M. J., Cordier, C., Dumas-Gaudot, E., Gianinazzi, S., Barea, J. M., & Azcon-Aguilar, C. (2002). Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. Journal of Experimental Botany, 53, 525–534.CrossRefGoogle Scholar
  96. Prashanthi, S. K., Kulkarni, S., Sreenivasa, M. N., & Kulkarni, S. (1997). Integrated management of root rot disease of safflower caused by Rhizoctonia bataticola. Environment and Ecology, 15, 800–802.Google Scholar
  97. Puppi, G., Azcón, R., & Hoflich, G. (1994). Management of positive interactions of arbuscular mycorrhizal fungi with essential groups of soil microorganisms. In S. Gianinazzi & H. Schouepp (Eds.), Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems (pp. 201–215). Basel: Birkhäuser.CrossRefGoogle Scholar
  98. Rambelli, A. (1973). The rhizosphere of mycorrhizae. In G. L. Marks & T. T. Koslowski (Eds.), Ectomycorrhizae (pp. 299–343). New York: Academic.CrossRefGoogle Scholar
  99. Ratnayake, M., Leonard, R. T., & Menge, J. A. (1978). Root exudation in relation to supply of phosphorus and its possible relevance to mycorrhiza formation. The New Phytologist, 81, 543–552.CrossRefGoogle Scholar
  100. Ravnskov, S., & Jakobsen, I. (1995). Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. The New Phytologist, 129, 611–618.CrossRefGoogle Scholar
  101. Read, D. J., & Perez-Moreno, J. (2003). Mycorrhizas and nutrient cycling in ecosystems – A journey towards relevance? The New Phytologist, 157, 475–492.CrossRefGoogle Scholar
  102. Rhodes, L. H., & Gerdemann, J. W. (1975). Phosphate uptake zones of mycorrhizal and non-mycorrhizal onions. The New Phytologist, 75, 555–561.CrossRefGoogle Scholar
  103. Salvioli, A., & Bonfante, P. (2013). Systems biology and omics tools: A cooperation for next-generation mycorrhizal studies. Plant Science, 203–204, 107–114.PubMedCrossRefPubMedCentralGoogle Scholar
  104. Schaarschmidt, S., Gresshoff, P. M., & Hause, B. (2013). Analyzing the soybeantranscriptomeduringautoregulationofmycorrhizationidentifies the transcription factorsGmNF-YA1a/bas positive regulators of arbuscular mycorrhization. Genome Biology, 14, R62.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Schonbeck, F., & Spengler, G. (1979). The detection of TMV in mycorrhizal cells of the tomato plant by means of immunofluorescence. Phytopathologische Zeitschrift, 94, 84–86.CrossRefGoogle Scholar
  106. Schreiner, R. P., & Bethlenfalvay, G. J. (1997). Mycorrhizae, biocides, and biocontrol: 3. Effects of three different fungicides on developmental stages of three AM fungi. Biology and Fertility of Soils, 24, 18–26.CrossRefGoogle Scholar
  107. Schübler, A., & Walker, C. (2011). Evolution of the ‘plant-symbiotic’ fungal phylum, Glomeromycota. In S. Póggeler & J. Wostemeyer (Eds.), Evolution of fungi and fungal like organisms (pp. 163–185). Berlin/Heidelberg: Springer.CrossRefGoogle Scholar
  108. Schübler, A., Gehrig, H., Schwarzott, D., & Walker, E. (2001). Analysis of partial Glomales SSU rRNA gene sequences: Implications for primer design and phylogeny. Mycological Research, 105, 5–15.CrossRefGoogle Scholar
  109. Shalaby, A. M., & Hanna, M. M. (1998). Preliminary studies on interactions between VA mycorrhizal fungus Glomus mosseae, Bradyrhizobium japonicum and Pseudomonas syringae in soybean plants. Acta Microbiologica Polonica, 47, 385–391.Google Scholar
  110. Sharma, D. D., Govindaiah, S., Katiyar, R. S., Das, P. K., Janardhan, L., Bajpai, A. K., Choudhry, P. C., & Janardhan, L. (1995). Effect of VA-mycorrhizal fungi on the incidence of major mulberry diseases. Indian Journal of Sericulture, 34, 34–37.Google Scholar
  111. Sharma, S., Dohroo, N. P., & Sharma, S. (1997). Management of ginger yellows through organic amendment, fungicide seed treatment and biological methods. Indian Cocoa Arecanut Spice Journal, 21, 29–30.Google Scholar
  112. Shaul, O., Galili, S., Volpin, H., Ginzberg, I., Elad, Y., Chet, I., & Kapulnik, Y. (1999). Mycorrhiza-induced changes in disease severity and PR protein expression in tobacco leaves. Molecular Plant-Microbe Interactions, 12, 1000–1007.PubMedCrossRefPubMedCentralGoogle Scholar
  113. Sikora, R. A. (1997). Biological system management in the rhizosphere an inside-out/outside-in perspective. Mededelingen – Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen, Universiteit Gent, 62, 105–112.Google Scholar
  114. Sikora, R. A., Pocasangre, L., FeldeZum, A., Niere, B., Vu, T. T., & Dababat, A. A. (2008). Mutualistic endophytic fungi and in planta suppressiveness to plant-parasitic nematodes. Biological Control, 46, 15–23.CrossRefGoogle Scholar
  115. Singh, L. P., Gill, S. S., & Tuteja, N. (2011). Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signaling & Behavior, 6, 175–191.CrossRefGoogle Scholar
  116. Slezack, S., Dumas-Gaudot, E., Paynot, M., & Gianinazzi, S. (2000). Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches. Molecular Plant-Microbe Interactions, 13, 238–241.PubMedCrossRefPubMedCentralGoogle Scholar
  117. Smith, F. A., & Smith, S. E. (2011). What is the significance of the arbuscular mycorrhizal colonization of many economically important crop plants? Plant and Soil, 348, 63–79.CrossRefGoogle Scholar
  118. Smith, S. E., & Smith, F. A. (2012). Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia, 104, 1–13.PubMedCrossRefPubMedCentralGoogle Scholar
  119. Sood, G. S. (2003). Chemotactic response of plant-growth-promoting bacteria towards roots of vesicular-arbuscular mycorrhizal tomato plants. FEMS Microbiology Ecology, 45, 219–227.CrossRefGoogle Scholar
  120. Srnith, S. E., & Read, D. I. (2008). Mycorrhizal symbiosis (3rd ed.). New York: Elsevier/Academic.Google Scholar
  121. St-Arnaud, M., Hamel, C., Vimard, B., Caron, M., & Fortin, J. A. (1995). Altered growth of Fusarium oxysporum f. sp. chrysanthemiin an in vitro dual culture system with the vesicular ar366buscular mycorrhizal fungus Glomus intraradices growing on Daucus carota transformed roots. Mycorrhiza, 5, 431–438.Google Scholar
  122. Steinkellner, S., Lendzemo, V., Langer, I., Schweiger, P., Khaosaad, T., Toussaint, J.-P., et al. (2007). Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules, 12, 1290–1306.PubMedPubMedCentralCrossRefGoogle Scholar
  123. Stoffelen, R., Verlinden, R., Xuyen, N. T., DeWaele, D., & Swennen, R. (2000). Host plant response of Eumusa and Australimusa bananas(Musa spp.) to migratory endoparasitic and root-knot nematodes. Nematology, 2, 907–916.CrossRefGoogle Scholar
  124. Sundaresan, P., Raja, N. U., & Gunasekaran, P. (1993). Induction and accumulation of phytoalexins in cowpea roots infected with a mycorrhizal fungus Glomus fasciculatum and their resistance to Fusarium wilt disease. Journal of Biosciences, 18, 291–301.CrossRefGoogle Scholar
  125. Takahashi, T., Katano, H., & Yoshikawa, N. (1994). Evidence for vesicular-arbuscular mycorrhizal infection in viroid-infected hop root tissues. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz, 101, 267–271.Google Scholar
  126. Tisdall, J. M., & Oades, J. M. (1979). Stabilization of soil aggregates by the root systems of rye grass. Australian Journal of Soil Research, 17, 429–441.CrossRefGoogle Scholar
  127. Torres-Barragan, A., Zavaleta-Mejia, E., Gonzalez-Chavez, C., & Ferrera-Cerrato, R. (1996). The use of arbuscular mycorrhizae to control onion white rot (Sclerotium cepivorum Berk.) underfield conditions. Mycorrhiza, 6, 253–258.CrossRefGoogle Scholar
  128. Trotta, A., Varese, G. C., Gnavi, E., Fusconi, A., Sampo, S., & Berta, G. (1996). Interactions between the soil borne pathogen Phytophthora nicotianae var. parasitica and the arbuscular mycorrhizal fungus Glomus mosseae in tomato plants. Plant and Soil, 185, 199–209.CrossRefGoogle Scholar
  129. van der Heijden, M. G. A., Martin, F. M., Selosse, M. A., & Sanders, I. R. (2015). Mycorrhizal ecology and evolution: The past, the present, and the future. The New Phytologist, 205, 1406–1423.CrossRefGoogle Scholar
  130. VanEtten, H. D., Sandrock, R., Wasmann, C., Soby, S., Mccluskey, K., & Wang, P. (1995). Detoxification of phytoanticipins and phytoalexins by phytopathogenic fungi. Canadian Journal of Botany, 73, 518–525.CrossRefGoogle Scholar
  131. Vierheilig, H., Steinkellner, S., & Khaosaad, T. (2008). The biocontrol effect of mycorrhization on soilborne fungal pathogens and the autoregulation of the AM symbiosis: One mechanism, two effects? In A. Varma (Ed.), Mycorrhiza (pp. 307–320). Berlin: Springer.CrossRefGoogle Scholar
  132. Vinayak, K., & Bagyaraj, D. J. (1990). Vesicular-arbuscular mycorrhizae screened for Troyer citrange. Biology and Fertility of Soils, 9, 311–314.CrossRefGoogle Scholar
  133. Vos, C. (2012). Arbusculaire mycorrhizenschimmels in de biocontrole van plantenparasitaire nematoden. Leuven: University of Leuven (KULeuven).Google Scholar
  134. Vos, C. M., Yang, Y., DeConinck, B., & Cammue, B. P. A. (2014). Fungal(-like) biocontrol organisms in tomato disease control. Biological Control, 74, 65–81.CrossRefGoogle Scholar
  135. Waschkies, C., Schropp, A., & Marschner, H. (1994). Relations between grapevine replant disease and root colonization of grapevine (Vitis sp.) by fluorescent pseudomonads and endomycorrhizal fungi. Plant and Soil, 162, 219–227.CrossRefGoogle Scholar
  136. Wesemael, W., Viaene, N., & Moens, M. (2011). Root-knot nematodes (Meloidogyne spp.) in Europe. Nematology, 13, 3–16.CrossRefGoogle Scholar
  137. Wyss, P., Boller, T., & Wiemken, A. (1991). Phytoalexin response is elicited by a pathogen (Rhizoctonia solani) but not by a mycorrhizal fungus (Glomus mosseae) in soybean roots. Cellular and Molecular Life Sciences, 47(4), 395–399.CrossRefGoogle Scholar
  138. Xavier, L. J. C. (L. Johnny). (1999). Effects of interactions between arbuscular mycorrhizal fungi and Rhizobium leguminosarum on pea and lentil. PhD dissertation. Saskatoon: University of SaskatchewanGoogle Scholar
  139. Xavier, L. J. C., & Germida, J. J. (2003). Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biology and Biochemistry, 35, 471–478.CrossRefGoogle Scholar
  140. Yang, H., Zhang, Q., Dai, Y., Liu, Q., Tang, J., Bian, X., et al. (2014). Effects of arbuscular mycorrhizal fungi on plant growth depend on root system: A meta-analysis. Plant and Soil, 389, 361–374.CrossRefGoogle Scholar
  141. Zamioudis, C., & Pieterse, C. M. J. (2012). Modulation of host immunity by beneficial microbes. Molecular Plant-Microbe Interactions, 25, 139–150.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Pranay Jain
    • 1
  • Ram Kumar Pundir
    • 2
  1. 1.Faculty in Department of Biotechnology, University Institute of Engineering and Technology (UIET)Kurukshetra UniversityKurukshetraIndia
  2. 2.Faculty in Department of Biotechnology EngineeringAmbala College of Engineering and Applied Research (ACE)AmbalaIndia

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