Advertisement

Arbuscular Mycorrhizal Colonization and Activation of Plant Defense Responses Against Phytopathogens

  • Anupam Maharshi
  • Gagan Kumar
  • Arpan Mukherjee
  • Richa Raghuwanshi
  • Harikesh Bahadur Singh
  • Birinchi Kumar Sarma
Chapter

Abstract

Arbuscular mycorrhizal fungi (AMF) are potentially mutualistic biotrophs of plants and improve water supply and nutrient uptake in host plants. In exchange of this, it takes a part of photosynthate from the host plant to fulfill its metabolic requirements. Despite having its own immune system, plant gets attacked by various pathogens and therefore needs support to overcome such challenges and to become stabilized in such hostile environment. AMF colonization helps the plants either directly or indirectly to face the challenges of biotic and abiotic stresses. Several physiological and biochemical changes occur in the host plant and mycorrhizosphere following colonization of roots by AMF, and AMF colonization also affects interactions of the host plants with a diverse range of both above- and belowground organisms. Protective effects of AMF colonization against pests, pathogens, and stem or root parasitic plants were described in many agriculturally important crop species. These mechanisms not only improve plant nutrition consumption and competition but also play a significant role in plant defense activation. Successful establishment of mycorrhizal species on host leads to regulation of the JA and SA signaling pathways, and it itself explains the range of protection conferred by this symbiosis. Defense activation following colonization by mycorrhizal species is associated with moderate activation of host transcription factors such as MAP kinases. Further, several other defense-related compounds are also accumulated such as PR proteins, β-1,3-glucanases, phytoalexins, and phenolics, and deposition of callose also occurs leading to protection against various pathogens. In the present chapter, we discussed the major defense signaling aspects during plant-pathogen interactions mediated through mycorrhizal colonization in the host plant roots.

Keywords

Mycorrhizal colonization Pathogen Rhizosphere Microbial communities 

References

  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefPubMedCentralGoogle Scholar
  2. Alexander T, Toth R, Meier R, Weber HC (1989) Dynamics of arbuscule development and degeneration in onion, bean, and tomato with reference to vesicular-arbuscular mycorrhizas in grasses. Can J Bot 67:2505–2513CrossRefGoogle Scholar
  3. Auge R (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  4. Balestrini R, Berta G, Bonfante P (1992) The plant nucleus in mycorrhizal roots: positional and structural modifications. Biol Cell 75:235–243CrossRefGoogle Scholar
  5. Barea JM, Azcón-Aguilar C, Azcón R (1996) Interactions between mycorrhizal fungi and rhizosphere microorganisms within the context of sustainable soil-plant systems. In: Gange AC, Brown VK (eds) Multitrophic interactions in terrestrial systems. Blackwell, OxfordGoogle Scholar
  6. Barea JM, Azcon R, Azcon-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie Van Leeuwenhoek 81:343–351PubMedCrossRefPubMedCentralGoogle Scholar
  7. Berta G, Sgorbati S, Soler V, Fusconi A, Trotta A, Citterio A, Scannerini S (1990) Variations in chromatin structure in host nuclei of a vesicular arbuscular mycorrhiza. New Phytol 114:199–205CrossRefGoogle Scholar
  8. Bharadwaj DP, Lundquist PO, Alstrom S (2008) Arbuscular mycorrhizal fungal spore-associated bacteria affect mycorrhizal colonization, plant growth and potato pathogens. Soil Biol Biochem 40:2494–2501CrossRefGoogle Scholar
  9. Blee E (2002) Impact of phyto-oxylipins in plant defense. Trends Plant Sci 7:315–322PubMedCrossRefPubMedCentralGoogle Scholar
  10. Blee KA, Anderson AJ (1996) Defense-related transcript accumulation in Phaseolus vulgaris L. colonized by the arbuscular mycorrhizal fungus Glomos intraradices Schsnck & Smith. Plant Physiol 110:675–688PubMedPubMedCentralCrossRefGoogle Scholar
  11. Blee KA, Anderson AJ (2000) Defence responses in plants to arbuscular mycorrhizal fungi. In: Podilla GK, Douds DD (eds) Current advances in mycorrhizas research. The American Phytopathological society, St. Paul, pp 45–59Google Scholar
  12. Blilou I, Ocampo JA, García-Garrido JM (2000) Induction of Ltp (lipid transfer protein) and pal (phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J Exp Bot 51:1969–1977PubMedCrossRefGoogle Scholar
  13. Bodker L, Kjoller R, Rosendahl S (1998) Effect of phosphate and the arbuscular mycorrhizal fungus Glomus intra radices on disease severity of root rot of peas (Pisum sativum) caused by Aphanomyces euteiches. Mycorrhiza 8:169–174CrossRefGoogle Scholar
  14. Bolwell GP (2004) Role of active oxygen species and NO in plant defence responses. Curr Opin Plant Biol 2:287–294CrossRefGoogle Scholar
  15. Bonfante-Fasolo P, Perotto S (1992) Plant and endomycorrhizal fungi: the cellular and molecular basis of their interaction. In: Verma DPS (ed) Molecular signal in plant microbe communication. CRC Press, Boca Raton, pp 445–470Google Scholar
  16. Bonfante-Fasolo P, Scannerini S (1992) In: Allen MJ (ed) The cellular basis of plant-fungus interchanges in mycorrhizal associations. Chapman and Hall, New York, pp 65–101Google Scholar
  17. Cervantes-Gamez RG, Bueno-Ibarra MA, Cruz-Mendivil A, Calderon- Vazquez CL, Ramirez-Douriet CM, Maldonado-Mendoza IE et al (2015) Arbuscular mycorrhizal symbiosis-induced expression changes in Solanum lycopersicum leaves revealed by RNA- seqanalysis. Plant Mol Biol Rep 23:1–14Google Scholar
  18. Christie P, Li X, Chen B (2004) Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant Soil 261(1–2):209–217CrossRefGoogle Scholar
  19. Collinge DB, Gregersen PL, Thordal-Christensen H (1994) The induction of gene expression in response to pathogenic microbes. In: Perspectives ASB (ed) Mechanisms of plant growth and lmproved productivity: modern approaches and. Marcel Dekker, New York, pp 391–433Google Scholar
  20. Comino C, Hehn A, Moglia A, Menin B, Bourgaud F, Lanteri S, Portis E (2009) The isolation and mapping of a novel hydroxycinnamoyltransferase in the globe artichoke chlorogenic acid pathway. BMC Plant Biol 9:30PubMedPubMedCentralCrossRefGoogle Scholar
  21. Conrath U, Beckers GJ, Flors V, Garcia-Agustín P, Jakab G, Mauch F, Newman MA, Pieterse CM, Poinssot B, Pozo MJ, Pugin A (2006) Priming: getting ready for Battle. Mol Plant-Microbe Interact 19:1062–1071PubMedCrossRefGoogle Scholar
  22. Copetta A, Lingua G, Berta G (2006) Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese. Mycorrhiza 16:485–494PubMedCrossRefGoogle Scholar
  23. Cordier C, Gianinazzi S, Gianinazzi-Pearson V (1996) Colonisation patterns of roots tissues by Phytophthora nicotianae var. parasitica related to reduced disease in mycorrhizal tomato. Plant Soil 185:223–232CrossRefGoogle Scholar
  24. Cordier C, Pozo MJ, Barea JM, Gianinazzi 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. Mol Plant-Microbe Interact 11:1017–1028CrossRefGoogle Scholar
  25. De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17:349–359PubMedCrossRefGoogle Scholar
  26. De Leon IP, Sanz A, Hamberg M, Castresana C (2002) Involvement of the Arabidopsis α-DOX1 fatty acid dioxygenase in protection against oxidative stress and cell death. Plant J 29:61–62PubMedCrossRefGoogle Scholar
  27. Dehne HW (1982) Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathology 72:1115–1119Google Scholar
  28. Delledonne M, Murgia I, Ederle D, Sbicego PF, Biondian A, Polverari A, Lamb C (2002) Reactive oxygen intermediates modulates nitric oxide signaling in the plant hypersensitive disease-resistance response. Plant Physiol Biochem 40:605–610CrossRefGoogle Scholar
  29. Dixon RA, Harrison MJ (1990) Activation, structure and organization of genes involved in microbial defense in plants. Adv Genet 28:165–234PubMedCrossRefPubMedCentralGoogle Scholar
  30. Dumas-Gaudot E, Asselin A, Gianinaui-Pearson V, Gollotte A, Gianinaui S (1994) Chitinase isoforms in roots of various pea genotypes infected with arbuscular mycorrhizal fungi. Plant Sci 99:27–37CrossRefGoogle Scholar
  31. Dumas-Gaudot E, Gollotte A, Ordier C, Gianinazzi S, Gianinazzi-Pearson V (2000) Modulation of host defence systems. In Arbuscular mycorrhizas: physiology and function, Kluwer Academic Publishers, Dordrecht, pp 173–200CrossRefGoogle Scholar
  32. El- Khallal SM (2007) Induction and modulation of resistance in tomato plants against Fusarium wilt disease by bioagent fungi (arbuscular mycorrhiza) and/or hormonal elicitors (Jasmonic acid & Salicylic acid): 2-Changes in the antioxidant enzymes, phenolic compounds and pathogen related proteins. Aust J Basic Appl Sci 1:717–732Google Scholar
  33. Engstrom K, Widmark AK, Brishammar S, Helmersoon S (1999) Antifungal activity to Phytophthora infestans of sesquiterpenoids from infected potato tubers. Potato Res 42:43–50CrossRefGoogle Scholar
  34. Evans DG, Miller MH (1988) Vesicular arbuscular mycorrhizas and the soil induced reduction of nutrient absorption in maize, casual relation. New Phytol 110:67–74CrossRefGoogle Scholar
  35. Feussner I, Kühn H, Wasternack C (2001) Lipoxygenase dependent degradation of storage lipids. Trends Plant Sci 6:268–273PubMedCrossRefGoogle Scholar
  36. Franken P, Gnadinger F (1994) Analysis of parsley arbuscular endomycorrhiza: lnfection development and mRNA levels of defense related genes. Plant-Microbe Interact 7:612–620CrossRefGoogle Scholar
  37. Fritz M, Jakobsen I, Lyngkjaer MZ, Thordal-Christensen H, Pons Kuhnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419PubMedCrossRefGoogle Scholar
  38. Garcia-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386PubMedCrossRefPubMedCentralGoogle Scholar
  39. Garcia-Gonzalez I, Quemada M, Gabriel JL, Hontoria C (2016) Arbuscular mycorrhizal fungal activity responses to winter cover crops in a sunflower and maize cropping system. Appl Soil Ecol 102:10–18CrossRefGoogle Scholar
  40. Garmendia I, Aguirreolea J, Goicoechea N (2006) Defence-related enzymes in pepper roots during interactions with arbuscular mycorrhizal fungi and/or Verticillium dahliae. BioControl 51:293–310CrossRefGoogle Scholar
  41. Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528–534Google Scholar
  42. Gaur A, Adholeya A (2002) Arbuscular–mycorrhizal inoculation of five tropical fodder crops and inoculum production in marginal soil amended with organic matter. Biol Fertil Soils 35:214–218CrossRefGoogle Scholar
  43. Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ 113:17–35CrossRefGoogle Scholar
  44. Grant C, Bittman S, Montreal M, Plenchette C, Morel C (2005) Soil and fertilizer phosphorus: effects on plant P supply and mycorrhizal development. Can J Plant Sci 85:3–14CrossRefGoogle Scholar
  45. Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant-Microbe Interact 22:763–772CrossRefGoogle Scholar
  46. Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220PubMedCentralCrossRefGoogle Scholar
  47. Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110CrossRefGoogle Scholar
  48. Howe GA, Schilmiller AL (2002) Oxylipin metabolism in response to stress. Curr Opin Plant Biol 5:230–236PubMedCrossRefPubMedCentralGoogle Scholar
  49. Jiao H, Yinglong C, Lin X, Liu R (2011) Diversity of arbuscular mycorrhizal fungi in greenhouse soils continuously planted to watermelon in North. China. Mycorrhiza 21:681–688PubMedCrossRefPubMedCentralGoogle Scholar
  50. Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13PubMedCrossRefPubMedCentralGoogle Scholar
  51. Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226(2):227–234CrossRefGoogle Scholar
  52. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizo deposition. New Phytol 163:459–480CrossRefGoogle Scholar
  53. Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664PubMedCrossRefPubMedCentralGoogle Scholar
  54. Kaldorf M, Kuhn AJ, Schroder WH, Hildebrandt U, Bothe H (1999) Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 154:718–728CrossRefGoogle Scholar
  55. Kapoor R, Bhatnagar AK (2007) Attenuation of cadmium toxicity in mycorrhizal celery (Apium graveolens L.). World J Microbiol Biotechnol 23:1083–1089CrossRefGoogle Scholar
  56. Khan AG (1993) Occurrence and importance of mycorrhizas in aquatic trees of New South Wales Australia. Mycorrhiza 3:31–38CrossRefGoogle Scholar
  57. Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21:1204–1209PubMedCrossRefPubMedCentralGoogle Scholar
  58. Kobayashi I, Kobayashi Y, Yamaoka N, Kunoh H (1992) Recognition of a pathogen and a nonpathogen by barley coleoptile cells. III. Responses of microtubules and actin filaments in barley coleoptile cells to penetration attempts. Can J Bot 70(9):1815–1823CrossRefGoogle Scholar
  59. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GED (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci U S A 105:9823–9828PubMedPubMedCentralCrossRefGoogle Scholar
  60. Künkel BN, Brooks DM (2002) Cross talk between signaling pathway in pathogen defense. Curr Opin Plant Biol 5:325–331PubMedCrossRefPubMedCentralGoogle Scholar
  61. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–257PubMedCrossRefPubMedCentralGoogle Scholar
  62. Lambais MR (2000) Regulation of plant defence-related genes in arbuscular mycorrhizas. In: Podilla GK, Douds DD (eds) Current advances in mycorrhizas research. The American Phytopathological Society, St. Paul, pp 45–59Google Scholar
  63. Landwehr M, Hildebrandt U, Wilde P, Nawrath K, Tóth T, Biró B, Bothe H (2002) The arbuscular mycorrhizal fungus Glomus geosporum in European saline, sodic and gypsum soils. Mycorrhiza 12:199–211PubMedCrossRefPubMedCentralGoogle Scholar
  64. Leon Morcillo RJ, Ocampo JA, Garcia Garrido JM (2012) Plant 9-lox oxylipin metabolism in response to arbuscular mycorrhiza. Plant Signal Behavior 7:1584–1588CrossRefGoogle Scholar
  65. Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C, Debelle F (2004) A putative Ca2+ and calmodulin dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364PubMedCrossRefPubMedCentralGoogle Scholar
  66. Li HY, Yang GD, Shu HR, Yang YT, Ye BX, Nishida I, Zheng CC (2006) Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in the grapevine (Vitis amurensis Rupr.), which includes transcriptional activation of the class III chitinase gene VCH3. Plant Cell Physiol 47:154–163PubMedCrossRefPubMedCentralGoogle Scholar
  67. Linderman RG (1994) Role of VAM fungi in biocontrol. In: Pfleger FL, Linderman RG (eds) Mycorrhizae and plant health. APS, St Paul, pp 1–26Google Scholar
  68. 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 Biol Biochem 40:2217–2224CrossRefGoogle Scholar
  69. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544PubMedCrossRefPubMedCentralGoogle Scholar
  70. Lohse S, Schliemann W, Ammer C, Kopka J, Strack D, Fester T (2005) Organization and metabolism of plastids and mitochondria in arbuscular mycorrhizal roots of Medicago truncatula. Plant Physiol 139:329–340PubMedPubMedCentralCrossRefGoogle Scholar
  71. Lopez-Raez JA, Charnikhova T, Fernández I, Bouwmeester H, Pozo MJ (2011) Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 168:294–297PubMedCrossRefPubMedCentralGoogle Scholar
  72. Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol 8:532–540PubMedCrossRefPubMedCentralGoogle Scholar
  73. Ludwig-Muller J (2000) Hormonal balance in plants during colonization be mycorrhizal fungi. In: Kapulnik Y, Douds D (eds) Arbuscular mycorrhizas: physiology and function. Kluwer Academic Publishers, Amsterdam, pp 263–283CrossRefGoogle Scholar
  74. Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Puhler A, Perlick A, Kuster H (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol Plant-Microbe Interact 17:1063–1077PubMedCrossRefPubMedCentralGoogle Scholar
  75. Marin M, Ybarra M, Fe A, Garcia-Ferriz L (2002) Effect of arbuscular mycorrhizal fungi and pesticides on Cynara cardunculus growth. Agric Food Sci Finland 11:245–251CrossRefGoogle Scholar
  76. McArthur DA, Knowles NR (1992) Resistance responses of potato to vesicular-arbuscular mycorrhizal fungi under varying abiotic phosphorus levels. Plant Physiol 100:341–351PubMedPubMedCentralCrossRefGoogle Scholar
  77. McGonigle TP, Miller MH (1999) Winter survival of extra radical hyphae and spores of arbuscular mycorrhizal fungi in the field. Appl Soil Ecol 12:41–50CrossRefGoogle Scholar
  78. Meixner C, Ludwig-Muller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222:709–715PubMedCrossRefPubMedCentralGoogle Scholar
  79. Menendez AB, Scervino JM, Godeas AM (2001) Arbuscular mycorrhizal populations associated with natural and cultivated vegetation on a site of Buenos Aires province. Argent. Biol. Fertil Soil 33:373–381CrossRefGoogle Scholar
  80. Meyer JR, Linderman RG (1986) Response of subterranean clover to dual inoculation with vesicular-arbuscular mycorrhizal fungi and a plant growth-promoting bacterium, Pseudomonas putida. Soil Biol Biochem 18:185–190CrossRefGoogle Scholar
  81. Miller MH, McGonigle TP, Addy HD (1995) Functional ecology if vesicular arbuscular mycorrhizas as influenced by phosphate fertilization and tillage in an agricultural ecosystem. Crit Rev Biotechnol 15:241–255CrossRefGoogle Scholar
  82. Miranda JCC, Harris PJ (1994) Effects of soil P on spore germination and hyphal growth of fungi. New Phytol 128:103–108CrossRefGoogle Scholar
  83. Morton JB, Benny GL (1990) Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae with an emendation of Glomaceae. Mycotaxon 37:471–492Google Scholar
  84. Mozafar A, Anken T, Ruh R, Frossard E (2000) Tillage intensity, mycorrhizal and non mycorrhizal fungi and nutrient concentrations in maize, wheat and canola. Agron J 92:1117–1124CrossRefGoogle Scholar
  85. Muller J, Staehelin C, Xie JP, Neuhaus-Url G, Boller T (2000) Nod factors and chitooligomers elicit an increase in cytosolic calcium in aequorin expressing soybean cells. Plant Physiol 124:733–740PubMedPubMedCentralCrossRefGoogle Scholar
  86. Navazio L, Baldan B, Moscatiello R, Zuppini A, Woo SL, Mariani P, Lorito M (2007) Calcium-mediated perception and defense responses activated in plant cells by metabolite mixtures secreted by the biocontrol fungus Trichoderma atroviride. BMC Plant Biol 7:41–49PubMedPubMedCentralCrossRefGoogle Scholar
  87. Njeru EM, Avio L, Bocci G, Sbrana C, Turrini A, Barberi P, Giovannetti M, Oehl F (2015) Contrasting effects of cover crops on ‘hot spot’ arbuscular mycorrhizal fungal communities in organic tomato. Biol Fertil Soils 51:151–166CrossRefGoogle Scholar
  88. Owen D, Williams AP, Griffith GW, Withers PJA (2015) Use of commercial bio-inoculants to increase agricultural production through improved phosphorus acquisition. Appl Soil Ecol 86:41–54CrossRefGoogle Scholar
  89. Plenchette C, Furlan V, Fortin JA (1982) Comparative effects of different endomycorrhizal fungi on five host plants grown on calcined montmorillonite clay. J Am Soc Hortic Sci 107:535–538Google Scholar
  90. Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398CrossRefGoogle Scholar
  91. Pozo MJ, Azcón-Aguilar C, Dumas-Gaudot E, Barea JM (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 Sci 141:149–157CrossRefGoogle Scholar
  92. Pozo MJ, Loon LCV, Pieterse CMJ (2004) Jasmonates – signals in plant–microbe interactions. J Plant Growth Regul 23:211–222Google Scholar
  93. Pozo MJ, Verhage A, García-Andrade J, García JM, Azcón-Aguilar C (2009) Priming plant defence against pathogens by arbuscular mycorrhizal fungi. In: Mycorrhizas-functional processes and ecological impact. Springer, Berlin/Heidelberg, pp 123–135CrossRefGoogle Scholar
  94. Prost I, Dhondt S, Rothe G, Vicente J, Rodriguez MJ, Kift N (2005) Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol 139:1902–1913PubMedPubMedCentralCrossRefGoogle Scholar
  95. Rouphael Y, Cardarelli M, Colla G (2015) Role of arbuscular mycorrhizal fungi in alleviating the adverse effects of acidity and aluminium toxicity in zucchini squash. Sci Horticult 188:97–105CrossRefGoogle Scholar
  96. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317PubMedCrossRefGoogle Scholar
  97. Ruiz-Lozano JM, Roussel H, Gianinazzi S, Gianinazzi-Pearson V (1999) Defense genes are differentially induced by a mycorrhizal fungus and Rhizobium sp. in wild-type and symbiosis-defective pea genotypes. Mol Plant-Microbe Interact 12:976–984CrossRefGoogle Scholar
  98. Salzer P, Boller T (2000) Elicitor-induced reactions in mycorrhizas and their suppression. In: Podila GK, Douds DD (eds) Current advances in mycorrhizas research. The American Phytopathological Society, St. Paul, pp 1–10Google Scholar
  99. Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377PubMedCrossRefGoogle Scholar
  100. Schliemann W, Ammer C, Strack D (2008) Metabolite profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry 69:112–146CrossRefGoogle Scholar
  101. Secilia J, Bagyaraj DJ (1987) Bacteria and actinomycetes associated with pot cultures of vesicular-arbuscular mycorrhizas. Can J Microbiol 33:1069–1073CrossRefGoogle Scholar
  102. Sengupta A, Chaudhuri S (2002) Arbuscular mycorrhizal relations of mangrove plant community at the Ganges river estuary in India. Mycorrhiza 12:169–174PubMedCrossRefGoogle Scholar
  103. Sheng PP, Liu RJ, Li M (2012) Inoculation with an arbuscular mycorrhizal fungus and intercropping with pepper can improve soil quality and watermelon crop performance in a system previously managed by monoculture. Am Eurasian J Agri Environ Sci 12:1462–1468Google Scholar
  104. Siedow JN (1991) Plant lipoxygenase: structure and function. Annu Rev Plant Physiol Plant Mol Biol 42:145–188CrossRefGoogle Scholar
  105. Singh RK, Dai O, Nimasow G (2011) Effect of arbuscular mycorrhizal (AM) inoculation on growth of chili plant in organic manure amended soil. Afr J Micorbiol Res 28:5004–5012Google Scholar
  106. Smith GS (1987) Interactions of nematodes with mycorrhizal fungi. In: Veech JA, Dickon DW (eds) Vistas on nematology. Society of Nematology, Hyattsville, pp 292–300Google Scholar
  107. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  108. Smith FA, Smith SE (2011) What is the significance of the arbuscular mycorrhizal colonisation of many economically important crop plants. Plant Soil 348:63–79CrossRefGoogle Scholar
  109. Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:786PubMedPubMedCentralGoogle Scholar
  110. Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306PubMedPubMedCentralCrossRefGoogle Scholar
  111. Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci U S A 97:10625–10630PubMedPubMedCentralCrossRefGoogle Scholar
  112. Strange RN (2003) Introduction to plant pathology. Wiley, EnglandGoogle Scholar
  113. Strittmatter G, Gheysen G, Gianinaui-Pearson V, Hahn K, Niebel A, Rohde W, Tacke E (1996) Infections with various types of organisms stimulate transcription from a short promoter fragment of the potato gstl gene. Mol Plant-Microbe Interact 9:68–73PubMedCrossRefPubMedCentralGoogle Scholar
  114. Stumpe M, Carsjens JG, Stenzel I, Gobel C, Lang I, Pawlowski K, Hause B, Feussner I (2005) Lipid metabolism in arbuscular mycorrhizal roots of Medicago truncatula. Phytochemistry 66:781–791PubMedCrossRefPubMedCentralGoogle Scholar
  115. Subramanian KS, Charest C (1999) Acquisition of N by external hyphae of an arbuscular mycorrhizal fungus and its impact on physiological response in maize under drought-stressed and well-watered conditions. Mycorrhiza 9:69–75CrossRefGoogle Scholar
  116. Titus JH, Titus PJ, Nowak RS, Smith SD (2002) Arbuscular mycorrhizas of Mojave Desert plants. Western N Amer Naturalist 62:327–334Google Scholar
  117. Torres MA, Jonathan DG, Dangl JL (2006) Reactive oxygen species signalling in response to pathogen. Plant Physiol 141:373–378Google Scholar
  118. Toussaint J, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17:291–297CrossRefGoogle Scholar
  119. Vestberg M, Kahiluoto H, Wallius E (2011) Arbuscular mycorrhizal fungal diversity and species dominance in a temperate soil with long-term conventional and low-input cropping systems. Mycorrhiza 21:351–361PubMedCrossRefPubMedCentralGoogle Scholar
  120. Vierheilig H, Piche Y (2002) Signalling in arbuscular mycorrhiza: facts and hypotheses. In: Buslig B, Manthey J (eds) Flavonoids in cell functions. Kluwer Academic/Plenum Publishers, New York, pp 23–39CrossRefGoogle Scholar
  121. Vierheilig H, Alt M, Mohr U, Boller T, Wiemken A (1994) Ethylene biosynthesis and activities of chitinase and β-1,3-glucanase in the roots of host and non-host plants of vesicular-arbuscular mycorrhizal fungi after inoculation with Glomus mosseae. J Plant Physiol 143:337–343CrossRefGoogle Scholar
  122. Vos CM, Yang Y, DeConinck B, Cammue BPA (2014) Fungal (−like) biocontrol organisms in tomato disease control. Biol Control 74:65–81CrossRefGoogle Scholar
  123. Waaland ME, Allen EB (1987) Relationships between VA mycorrhizal fungi and plant cover following surface mining in Wyoming. J Range Manag 40:271–276CrossRefGoogle Scholar
  124. Wasternack C, Hause B (2002) Jasmonates and octadecanoids: signals in plant stress responses and development. Prog Nucleic Acid Res Mol Biol 72:165–221Google Scholar
  125. Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Canad J Bot 82:1198–1227CrossRefGoogle Scholar
  126. Zhu HH, Yao Q (2004) Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibit Ralstonia Solanacearum. J Phytopathol 152:537–546CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Anupam Maharshi
    • 1
  • Gagan Kumar
    • 1
  • Arpan Mukherjee
    • 2
  • Richa Raghuwanshi
    • 2
  • Harikesh Bahadur Singh
    • 1
  • Birinchi Kumar Sarma
    • 1
  1. 1.Department of Mycology and Plant Pathology, Institute of Agricultural SciencesBanaras Hindu UniversityVaranasiIndia
  2. 2.Department of Botany, Institute of ScienceBanaras Hindu UniversityVaranasiIndia

Personalised recommendations