The Use of Arbuscular Mycorrhizal Fungi in Combination with Trichoderma spp. in Sustainable Agriculture

  • Jose Antonio PascualEmail author


Arbuscular mycorrhizal (AM) fungi as well as fungal biological control agent such as Trichoderma spp. have shown beneficial effects on plant growth and health. The study of the interactions between AM fungi, fungal antagonists and plants is of great interest. Before using them, it is in fact important to understand whether and how the two different beneficial fungal components can influence each other and/or the host plant. In this chapter, the attention is focused on the plant responses to the inoculation with AM fungi and Trichoderma spp., alone or in combination, with particular attention to the impact on the plant hormonal balance.


Salicylic Acid Arbuscular Mycorrhizal Indole Acetic Acid Jasmonic Acid Induce Systemic Resistance 
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.


  1. Abeles FB, Morgan PW, Saltveit ME Jr (1992) Ethylene in plant biology. Academic, San DiegoGoogle Scholar
  2. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827CrossRefPubMedGoogle Scholar
  3. Altomare C, Norvell WA, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant–growth promoting and biocontrol fungus Trichoderma harzianum Rifai 1295–22. Appl Environ Microbiol 65:2926–2933PubMedPubMedCentralGoogle Scholar
  4. Avis TJ, Gravel V, Antoun H, Tweddell RJ (2008) Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol Biochem 40:1733–1740CrossRefGoogle Scholar
  5. Azcón–Aguilar C, Bago B (1994) Physiological characteristics of the host plant promoting and undisturbed functioning of the mycorrhizal symbiosis. In: Gianinazzi S, Schepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhauser, BaselGoogle Scholar
  6. Azcón–Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil–borne plant pathogens – an overview of the mechanisms involved. Mycorrhiza 6:457–464Google Scholar
  7. Barea JM, Azcón–Aguilar C, Azcón R (1997) 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 Science, CambridgeGoogle Scholar
  8. Barea JM, Azcón R, Azcón–Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Anton Leeuw 81:343–351CrossRefGoogle Scholar
  9. Benítez T, Rincón AM, Limón Antonio MC, Codón C (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260PubMedGoogle Scholar
  10. Bi HH, Song YY, Zeng RS (2007) Biochemical and molecular responses of host plants to mycorrhizal infection and their roles in plant defense. Allelopathy J 29:15–27Google Scholar
  11. Brimner T, Boland GJ (2003) A review of the non–target effects of fungi used to biologically control plant diseases. Agric Ecosyst Environ 100:3–16CrossRefGoogle Scholar
  12. Calvet C, Barea JM, Pera J (1992) In Vitro interactions between the vesicular–arbuscular mycorrhizal fungus Glomus mosseae and some saprophytic fungi isolated from organic substrates. Soil Biol Biochem 8:775–780CrossRefGoogle Scholar
  13. Calvet C, Pera J, Barea JM (1993) Growth response of marigold (Tagetes erecta L.) to inoculation with Glomus mosseae, Trichoderma aureoviride and Pythium ultimum in a peat–perlite mixture. Plant Soil 148:1–6CrossRefGoogle Scholar
  14. Campos–Soriano L, García–Martínez J, San Segundo B (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence–related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13:579–592CrossRefPubMedGoogle Scholar
  15. Camprubí A, Calvet C, Estaún V (1995) Growth enhancement of Citrus reshni after inoculation with Glomus intraradices and Trichoderma aureoviride and associated effects on microbial population and enzyme activity in potting mixes. Plant Soil 173:233–238CrossRefGoogle Scholar
  16. Caron M (1989) Potential use of mycorrhizae in control of plant borne diseases. Can J Plant Pathol 11:177–179CrossRefGoogle Scholar
  17. Chet I (1987) Trichoderma – application, mode of action, and potential as a biocontrol agent of soilborne plant pathogenic fungi. In: Chet I (ed) Innovative approaches to plant disease control. Wiley, New YorkGoogle Scholar
  18. Chet I, Inbar J, Hadar Y (1997) Fungal antagonists and mycoparasites. In: Wicklow S (ed) Mycota environmental and microbial relationships, vol IV. Springer–Verlag, Berlin, pp 165–184Google Scholar
  19. Contreras–Cornejo HA, Macías–Rodríguez L, CortésPenagos C, López–Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin–dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592CrossRefPubMedPubMedCentralGoogle Scholar
  20. Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi– Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant Microbe Interact 11:1017–1028CrossRefGoogle Scholar
  21. De Meyer G, Bigirimana J, Elad Y, Höfte M (1998) Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. Eur J Plant Pathol 104:279286CrossRefGoogle Scholar
  22. De Silva A, Patterson K, Rothrock C, Moore J (2000) Growth promotion of highbush blueberry by fungal and bacterial inoculants. Hortscience 35:1228–1230Google Scholar
  23. Fernández I, Merlos M, López–Ráez JA, Martínez–Medina A, Ferrol N, Azcón C, Bonfante P, Flors V, Pozo MJ (2014) Defense related phytohormones regulation in arbuscular mycorrhizal symbioses depends on the partner genotypes. J Chem Ecol 40:791–803CrossRefPubMedGoogle Scholar
  24. Filion M, St–Arnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhiza fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol 141:525533CrossRefGoogle Scholar
  25. Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell–type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987CrossRefPubMedGoogle Scholar
  26. Foo E, Ross JJ, Jones WT, Reid JB (2013) Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 111:769–779CrossRefPubMedPubMedCentralGoogle Scholar
  27. Fracchia S, Mujica MT, García–Romera I, GarcíaGarrido JM, Martin J, Ocampo JA, Godeas A (1998) Interactions between Glomus mosseae and arbuscular mycorrhizal sporocarp–associated saprophytic fungi. Plant Soil 200:131–137CrossRefGoogle Scholar
  28. Gao LL, Knogge W, Delp G, Smith FA, Smith FS (2004) Expression patterns of defense–related genes in different types of arbuscular mycorrhizal development in wild–type and mycorrhiza–defective mutant tomato. Mol Plant-Microbe Interact 17:1103–1113CrossRefPubMedGoogle Scholar
  29. Garmendia I, Aguirreolea J, Goicoechea N (2005) Defence–related enzymes in pepper roots during interactions with arbuscular mycorrhizal fungi and or Verticillium dahliae. Biocontrol 51:293–310CrossRefGoogle Scholar
  30. Godeas A, Fracchia S, Mujica MT, Ocampo JA (1999) Influence of soil impoverishment on the interaction between Glomus mosseae and saprobe fungi. Mycorrhiza 9:185–189CrossRefGoogle Scholar
  31. Gravel V, Antoun H, Tweddell RJ (2007) Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biol Biochem 39:1968–1977CrossRefGoogle Scholar
  32. Green H, Larsen J, Olsson PA, Jensen DF, Jakobsen I (1999) Suppression of the biocontrol agent Trichoderma harzianum by mycelium of the arbuscular mycorrhizal fungus Glomus intraradices in root–free soil. Appl Environ Microbiol 65:1428–1434PubMedPubMedCentralGoogle Scholar
  33. Grunwald U, Guo W, Fischer K, Isayenkov S, Ludwig–Mueller J, Hause B, Yan X, Küster H, Franken P (2009) Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular mycorrhizal, Pi–fertilised and phytohormone–treated Medicago truncatula roots. Planta 229:1023–1034CrossRefPubMedPubMedCentralGoogle Scholar
  34. Gutjahr C (2014) Phytohormone signaling in arbuscular mycorrhiza development. Curr Opin Plant Biol 20:26–34CrossRefPubMedGoogle Scholar
  35. Haas JH, Krikun J (1985) Efficacy of endomycorrhizal–fungus isolates and inoculum quantities required for growth response. New Phytol 100:613–621CrossRefGoogle Scholar
  36. Haggag WM, Abd–El–Latif FM (2001) Interaction between vesicular arbuscular mycorrhizae and antagonistic biocontrol microorganisms on controlling root rot disease incidence of geranium plants. On Line J Biol Sci 1:1147–1153CrossRefGoogle Scholar
  37. Hanson LE, Howell CR (2004) Elicitors of plant defense responses from biological control strains of Trichoderma virens. Phytopathology 94:171–176CrossRefPubMedGoogle Scholar
  38. Harman GE (2000) Myth and dogmas of biocontrol changes in perceptions derived from research on Trichoderma harzianum T–22. Plant Dis 84:377–393CrossRefGoogle Scholar
  39. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:3456CrossRefGoogle Scholar
  40. Harrison MJ, Dixon RA (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol Plant-Microbe Interact 6:643–654CrossRefGoogle Scholar
  41. Harrison M, Dixon R (1994) Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago truncatula and the mycorrhizal fungus Glomus versiforme. Plant J 6:9–20Google Scholar
  42. Hause B, Maier W, Miersch O, Kramel R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (2000) Competition between roots and soil micro–organisms for nutrients from nitrogen–rich patches of varying complexity. J Ecol 88:150–164CrossRefGoogle Scholar
  44. Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10CrossRefGoogle Scholar
  45. Howell CR, Hanson LE, Stipanovic RD, Puckhaber LS (2000) Induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. Phytopathology 90:248–252CrossRefPubMedGoogle Scholar
  46. Jeffries, Barea JM (2001) Arbuscular mycorrhiza – a key component of sustainable plant–soil ecosystems. In: Hock B (ed) The mycota Vol. IX: fungal associations. Springer–Verlag, BerlinGoogle Scholar
  47. Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143CrossRefPubMedGoogle Scholar
  48. Kohler J, Caravaca F, Carrasco L, Roldan A (2007) Interactions between a plant–growth–promoting rhizobacterium, an AM fungus and a phosphate–solubilising fungus in the rhizosphere of Lactuca sativa. Appl Soil Ecol 35:480–487CrossRefGoogle Scholar
  49. Korolev N, David DR, Elad Y (2008) The role of phytohormones in basal resistance and Trichoderma–induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. Biocontrol 53:667–683CrossRefGoogle Scholar
  50. Lace B, Genre A, Woo S, Faccio A, Lorito M, Bonfante P (2014) Gate crashing arbuscular mycorrhizas: in vivimaging shows the extensive colonization of both symbionts by Trichoderma atroviride. Environ Microbiol Rep 7:64–67CrossRefPubMedGoogle Scholar
  51. Linderman RG (1992) Vesicular–arbuscular mycorrhizae and soil microbial interactions. In: Bethlenfalvay GJ, Linderman RG (eds) Mycorrhizae in sustainable agriculture, Special publication no. 54. Agronomy Society of America, MadisonGoogle Scholar
  52. 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 50:529–544CrossRefPubMedGoogle Scholar
  53. Ludwig–Müller J, Bennett R, García–Garrido J, Piché Y, Vierheilig H (2002) Reduced arbuscular mycorrhizal root colonization in Tropaeolum majus and Carica papaya after jasmonic acid application cannot be attributed to increased glucosinolate. J Plant Physiol 159:517–523CrossRefGoogle Scholar
  54. Marra R, Ambrosino P, Carbone V (2006) Study of the three–way interaction between Trichoderma atroviride, plant and fungal pathogens by using a proteomic approach. Curr Genet 50:307–321CrossRefPubMedGoogle Scholar
  55. Martinez C, Blanc F, Le Claire E, Besnard O, Nicole M, Baccou JC (2001) Salicylic acid and ethylene pathways are differentially activated in melon cotyledons by active or heat–denatured cellulase from Trichoderma longibrachiatum. Plant Physiol 127:334–344CrossRefPubMedPubMedCentralGoogle Scholar
  56. Martinez A, Obertello M, Pardo A, Ocampo JA, Godeas A (2004) Interactions between Trichoderma pseudokoningii strains and the arbuscular mycorrhizal fungi Glomus mosseae and Gigaspora rosea. Mycorrhiza 14:79–84CrossRefPubMedGoogle Scholar
  57. Martínez–Medina A, Pascual JA, Lloret E, Roldán A (2009) Interactions between arbuscular mycorrhizal fungi and Trichoderma harzianum and their effects on Fusarium wilt in melon plants grown in seedlings nurseries. J Sci Food Agric 89:1843–1850CrossRefGoogle Scholar
  58. Martínez–Medina, Pascual JA, Pérez–Alfocea F, Albacete A, Roldan A (2010) Trichoderma harzianum and Glomus intraradices modify the hormone disruption induced by Fusarium oxysporum infection in melon plants. Phythopathology 100:682–688CrossRefGoogle Scholar
  59. Martínez–Medina A, Roldán A, Pascual JA (2011) Interaction between arbuscular mycorrhizal fungi and Trichoderma harzianum under conventional and low input fertilization field condition in melon crops: growth response and Fusarium wilt biocontrol. Appl Soil Ecol 47:97–105Google Scholar
  60. Martínez–Medina, Fernández I, Sánchez–Guzmán MJ, Jung SC, Pascual JA, Pozo MJ (2013) Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Front Plant Sci 4:206PubMedPubMedCentralGoogle Scholar
  61. Martínez–Medina A, Alguacil MDM, Pascual JA, Van Wees SC (2014) Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth–promoting activity on melon plants. J Chem Ecol 40:804–815CrossRefPubMedGoogle Scholar
  62. McAllister CB, García–Romera I, Godeas A, Ocampo JA (1994) Interactions between Trichoderma koningii, Fusarium solani and Glomus mosseae: effects on plant growth, arbuscular mycorrhizas and the saprophyte inoculants. Soil Biol Biochem 26:1363–1367CrossRefGoogle Scholar
  63. McAllister CB, Garcia–Romera I, Martín J, Godeas A, Ocampo JA (1995) Interaction between Aspergillus niger van Tiegh and Glomus mosseae (Nicol and Gerd) Gerd & Trappe. New Phytol 129:309–316CrossRefGoogle Scholar
  64. McAllister CB, Garcia–Garrido JM, Garcia–Romera I, Godeas A, Ocampo JA (1996) In vitro interactions between Alternaria alternata, Fusarium equiseti and Glomus mosseae. Symbiosis 20:163–174Google Scholar
  65. McAllister CB, Garcia–Garrido JM, Garcia–Romera I, Godeas A, Ocampo JA (1997) Interaction between Alternaria alternata or Fusarium equiseti and Glomus mosseae and its effects on plant growth. Biol Fertil Soils 24:301–305CrossRefGoogle Scholar
  66. Meixner C, Ludwig–Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222:709–715CrossRefPubMedGoogle Scholar
  67. Pieterse CMJ, Van Pelt JA, Verhagen BWM, Ton J, van Wees SCM, Léon–Kloosterziel KM, van Loon LC (2003) Induced systemic resistance by plant growth promoting rhizobacteria. Symbiosis 35:3954Google Scholar
  68. Pozo MJ, Azcón–Aguilar C (2007) Unraveling mycorrhiza–induced resistance. Curr Opin Plant Biol 10:393–398CrossRefPubMedGoogle Scholar
  69. Pozo MJ, Cordier C, Dumas–Gaudot E, Gianinazzi S, Barea JM, Azcón–Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534CrossRefPubMedGoogle Scholar
  70. Pozo MJ, Verhage A, García–Andrade J, García JM, Azcón–Aguilar C (2009) Priming plant defence against pathogens by arbuscular mycorrhizal fungi. In: Azcón–Aguilar C, Barea JM, Gianinazzi S, Gianinazzi–Pearson V (eds) Mycorrhizas – functional processes and ecological impact. Springer, BerlinGoogle Scholar
  71. Ruzicka K, Ljung K, Vanneste S, Podhorsk’a R, Beeckman T, Friml J, Benková E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport dependent auxin distribution. Plant Cell 19:2197–2212CrossRefPubMedPubMedCentralGoogle Scholar
  72. Saldajeno MGB, Chandanie WA, Kubota M, Hyakumachi M (2008) Effects of interactions of arbuscular mycorrhizal fungi and beneficial saprophytic mycoflora on plant growth and disease protection. In: Siddiqui ZA, Akhtar MS, Futai K (eds) Mycorrhizae: sustainable agriculture and forestry. Springer Sciences, The NetherlandsGoogle Scholar
  73. Shoresh M, Yedidia I, Chet I (2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95:76–84CrossRefPubMedGoogle Scholar
  74. Siddiqui ZA, Mahmood I (1996) Biological control of Heterodera cajani and Fusarium udum on pigeonpea by Glomus mosseae, Trichoderma harzianum and Verticillium chlamydosporium. Isr J Plant Sci 44:49–56CrossRefGoogle Scholar
  75. Sticher L, Mauch–Mani B, Métraux JP (1997) Systemic acquired resistance. Anni Rev Phytopathol 35:235–270CrossRefGoogle Scholar
  76. Tarbell TJ, Koske RE (2007) Evaluation of commercial arbuscular mycorrhizal inocula in a sand/peat medium. Mycorrhiza 18:51–56CrossRefPubMedGoogle Scholar
  77. Toussaint JP (2007) Investigating physiological changes in the aerial parts of AM plants: what do we know and where should we be heading? Mycorrhiza 17:349–353CrossRefPubMedGoogle Scholar
  78. Tsavkelova EA, Cherdyntseva TA, Netrusov AI (2005) Auxin production by bacteria associated with orchid roots. Microbiology 74:46–53CrossRefGoogle Scholar
  79. Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P–solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71:137–144CrossRefPubMedGoogle Scholar
  80. Vázquez MM, César S, Azcón R, Barea JM (2000) Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl Soil Ecol 15:261–272CrossRefGoogle Scholar
  81. Vierheilig H (2004) Regulatory mechanisms during the plant–arbuscular mycorrhizal fungus interaction. Can J Bot 82:1166–1176CrossRefGoogle Scholar
  82. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Barbetti MJ, Li H, Woo SL, Lorito M (2008a) A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 72:80–86CrossRefGoogle Scholar
  83. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008b) Trichoderma–plant–pathogen interactions. Soil Biol Biochem 40:1–1CrossRefGoogle Scholar
  84. Volpin H, Elkind Y, Okon Y, Kapulnik Y (1994) A vesicular arbuscular mycorrhizal fungus Glomus intraradices induces a defence response in alfalfa roots. Plant Physiol 104:683–689PubMedPubMedCentralGoogle Scholar
  85. Volpin H, Phillips DA, Oken Y, Kapulnik Y (1995) Suppression of an isoflavonoid phytoalexin defense response in mycorrhizal alfalfa roots. Plant Physiol 108:1449–1454PubMedPubMedCentralGoogle Scholar
  86. Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227CrossRefGoogle Scholar
  87. Yedidia I, Shoresh M, Kerem Z, Benhamou N, Kapulnik Y, Chet I (2003) Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in Cucumber by Trichoderma asperellum (T–203) and accumulation of phytoalexins. Appl Environ Microbiol 69:7343–7353CrossRefPubMedPubMedCentralGoogle Scholar
  88. Zhu HH, Yao Q (2004) Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibits Ralstonia solanacearum. J Phytopathol 152:537–542CrossRefGoogle Scholar

Copyright information

© Springer India 2016

Authors and Affiliations

  1. 1.Centro de Edafología y Biología Aplicada del SeguraCEBAS-CSICMurciaSpain

Personalised recommendations