AM Fungi and Trichoderma Interaction for Biological Control of Soilborne Plant Pathogen Fusarium oxysporum



Fusarium oxysporum is an important soilborne destructive plant pathogen that has an effect on several plant species worldwide. The suggested practice for their effective control was the integration of several management practices, but it remains elusive till now. Since it is important to develop disease-resistant and high-yielding crops due to the increase in food demand with minimum utilization of natural resources, it is necessary that the prerequisite employment methodology be of biological origin and that the candidature for the role of biological control agents implies antagonists in various plant–microbe interactions such as arbuscular mycorrhizal fungi and Trichoderma spp. This review proposes a framework that might be helpful in the use of AM fungi and Trichoderma spp. for their effective biocontrol of several plant pathogens and insights into the mechanisms involved. Also, a relationship between arbuscular mycorrhizal fungi or Trichoderma spp. and the host plant is being emphasized upon for improved health and growth for production in present agricultural systems. Therefore, this review focuses on some approaches aimed at the biocontrol of F. oxysporum and biotechnological advancement involved in it for paving insights for future research.


Arbuscular mycorrhizal fungi Biological control agent Fusarium oxysporum Plant pathogen, Trichoderma 


Conflicts of Interest

The authors declare no competing and conflict of interest.


  1. Abdel-Fattah GM, El-Haddad SA, Hafez EE, Rashad YM (2011) Induction of defense responses in common bean plants by arbuscular mycorrhizal fungi. Microbiol Res 166:268–281PubMedCrossRefPubMedCentralGoogle Scholar
  2. Abhiram P, Masih H (2018) In vitro Antagonism of Trichoderma viride against Fusarium oxysporum strains. J Pharmacogn Phytochem 7:2816–2819Google Scholar
  3. Aboul-Soud MA, Yun BW, Harrier LA, Loake GJ (2004) Transformation of Fusarium oxysporum by particle bombardment and characterisation of the resulting transformants expressing a GFP transgene. Mycopathologia 158:475–482PubMedCrossRefPubMedCentralGoogle Scholar
  4. Agrios GN (1988) Plant pathology, 3rd edn. Academic, New York, p 803Google Scholar
  5. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefPubMedCentralGoogle Scholar
  6. Akkopru A, Demir S (2005) Biological control of Fusarium wilt in tomato caused by Fusarium oxysporum f. sp. lycopersici by AMF Glomus intraradices and some rhizobacteria. J Phytopathol 153:544–550CrossRefGoogle Scholar
  7. Alabouvette C, Lemanceau P, Steinberg C (1993) Recent advances in the biological control of Fusarium wilts. Pestic Sci 37:365–373CrossRefGoogle Scholar
  8. Alabouvette C, Olivain C, Migheli Q, Steinberg C (2009) Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt-inducing Fusarium oxysporum. New Phytol 184:529–544PubMedCrossRefPubMedCentralGoogle Scholar
  9. Al-Hazmi AS, Javeed MT (2016) Effects of different inoculum densities of Trichoderma harzianum and Trichoderma viride against Meloidogyne javanica on tomato. Saudi J Biol Sci 23:288–292PubMedCrossRefPubMedCentralGoogle Scholar
  10. Al-Hmoud G, Al-Momany A (2015) Effect of four mycorrhizal products on Fusarium root rot on different vegetable crops. J Plant Pathol Microb 6:255Google Scholar
  11. Alizadeh H, Behboudi K, Ahmadzadeh M, Javan-Nikkhah M, Zamioudis C, Pieterse CM, Bakker PA (2013) Induced systemic resistance in cucumber and Arabidopsis thaliana by the combination of Trichoderma harzianum Tr6 and Pseudomonas sp. Ps14. Biol Control 65:14–23CrossRefGoogle Scholar
  12. Amira MB, Lopeza D, Mohamedc AT, Khouajab A, Chaard H, Fumanala B, Gousset-Duponta A, Bonhommee L, Labela P, Goupila P, Ribeiroa S, Pujade-Renauda V, Juliena JL, Auguing D, Venissea JS (2017) Beneficial effect of Trichoderma harzianum strain Ths97 in bio-controlling Fusarium solani causal agent of root rot disease in olive trees. Biol Control 110:70–78CrossRefGoogle Scholar
  13. Andrabi M, Vaid A, Razdan VK (2011) Evaluation of different measures to control wilt causing pathogens in chickpea. J Plant Prot Res 51:55–59CrossRefGoogle Scholar
  14. Andrade SAL, Domingues AP, Mazzafera P (2015) Photosynthesis is induced in rice plants that associate with arbuscular mycorrhizal fungi and are grown under arsenate and arsenite stress. Chemosphere 134:141–149PubMedCrossRefGoogle Scholar
  15. Arabi MIE, Kanacri S, Ayoubi Z, Jawhar M (2013) Mycorrhizal application as a biocontrol agent against common root rot of barley. Res Biotechnol 4:07–12Google Scholar
  16. Atanasova L, Crom SL, Gruber S, Coulpier F, Seidl-Seiboth V, Kubicek CP, Druzhinina IS (2013) Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics 14:121PubMedPubMedCentralCrossRefGoogle Scholar
  17. Auge RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  18. Balaji LP, Ahir RR (2011) Evaluation of plant extracts and biocontrol agents against leaf spot disease of brinjal. Indian Phytopath 64:378–380Google Scholar
  19. Barea JM, Azcon-Aguilar C (1982) Production of plant growth-regulating substances by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Appl Environ Microbiol 43:810–813PubMedPubMedCentralGoogle Scholar
  20. Barker S, Tagu D (2000) The roles of auxins and cytokinins in mycorrhizal symbioses. J Plant Growth Regul 19:144–154PubMedGoogle Scholar
  21. Basu S, Rabara RC, Negi S (2018) AMF: the future prospect for sustainable agriculture. Physiol Mol Plant Pathol 102:36–45CrossRefGoogle Scholar
  22. Benitez T, Rincon AM, Limon MC, Codon AC (2004) Biocontrol mechanism of Trichoderma strains. Int Microbiol 7:249–260PubMedGoogle Scholar
  23. Berg A, Wangun H, Kemami V, Nkengfack AE, Schlegel B (2004) Lignoren, a new sesquiterpenoid metabolite from Trichoderma lignorum HKI 0257. J Basic Microbiol 44:317–319PubMedCrossRefGoogle Scholar
  24. Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1–13CrossRefGoogle Scholar
  25. Bhagat S, Pan S (2008) Variability in production of extra cellular hydrolytic enzymes by Trichoderma spp. and induction of disease resistance in gram (Ciccer arietinum). J Biol Conserv 22:57–66Google Scholar
  26. Bisby GR (1939) Trichoderma viride Pers. ex. Fries, and notes on Hypocrea. Trans Br Mycol Soc 33:149–168CrossRefGoogle Scholar
  27. Błaszczyk L, Siwulski M, Sobieralski K, Lisiecka J, Jędryczka M (2014) Trichoderma spp. – application and prospects for use in organic farming and industry. J Plant Prot Res 54:309–317CrossRefGoogle Scholar
  28. Blee KA, Anderson AJ (2000) Defense responses in plants to arbuscular mycorrhizal fungi. In: Podila GK, Douds DD Jr (eds) Current advances in mycorrhizae research. American Phytopathological Society Press, St. Paul, MN, pp 27–44Google Scholar
  29. Blilou I, Ocampo JA, Garcia-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
  30. Bohm H, Albert I, Fan L, Reinhard A, Nurnberger T (2014) Immune receptor complexes at the plant cell surface. Curr Opin Plant Biol 20:47–54PubMedCrossRefGoogle Scholar
  31. Braun H, Woitsch L, Hetzer B, Geisen R, Zange B, Schmidt-Heydt M (2018) Trichoderma harzianum: inhibition of mycotoxin producing fungi and toxin biosynthesis. Int J Food Microbiol 280:10–16PubMedCrossRefGoogle Scholar
  32. Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017PubMedCrossRefGoogle Scholar
  33. Brewer D, Taylor A, Keeping JW, Taha AA, Thaller V (1982) Production of experimental quantities of isocyanide metabolites of Trichoderma hamatum. Can J Microbiol 28:1252–1260PubMedCrossRefGoogle Scholar
  34. Brotman Y, Briff E, Viterbo A, Chet I (2008) Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 147:779–789PubMedPubMedCentralCrossRefGoogle Scholar
  35. Cangelosi B, Curir P, Beruto M, Monroy F, Borriello R (2017) Protective effects of arbuscular mycorrhizae against Fusarium Oxysporum F. Sp. Ranunculi in Ranunculus Asiaticus cultivations for flower crop. J Hortic Sci Res 1:36–41Google Scholar
  36. Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A, Stacey G (2014) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. elife 3:e03766PubMedCentralCrossRefPubMedGoogle Scholar
  37. Caron M, Fortin JA, Richard C (1986) Effect of inoculation sequence on the interaction between Glomus intraradices and Fusarium oxysporum f. sp. radicis-lycopersici in tomatoes. Can J Plant Pathol 8:12–16CrossRefGoogle Scholar
  38. Castellanos-Morales V, Keiser C, Cárdenas-Navarro R, Grausgruber H, Glauninger J, García-Garrido JM, Steinkellner S, Sampedro I, Hage-Ahmed K, Illana A, Ocampo JA, Vierheilig H (2011) The bioprotective effect of AM root colonization against the soil-borne fungal pathogen Gaeumannomyces graminis var. Tritici in barley depends on the barley variety. Soil Biol Biochem 43:831–834CrossRefGoogle Scholar
  39. Castillejo MA, Bani M, Rubiales D (2015) Understanding pea resistance mechanisms in response to Fusarium oxysporum through proteomic analysis. Phytochemistry 115:44–58PubMedCrossRefGoogle Scholar
  40. Cavagnaro TR, Bender SF, Asghari HR, van der Heijden MGA (2015) The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci 20:283–290PubMedCrossRefGoogle Scholar
  41. Chaudhary VB, Sandall EL, Lazarski MV (2018) Urban mycorrhizas: predicting arbuscular mycorrhizal abundance in green roofs. Fungal Ecol:1–8Google Scholar
  42. Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant-Microbe Interact 19:1062–1071PubMedCrossRefGoogle Scholar
  43. Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos C (2009) Trichoderma virens, a plant beneficial fungus enhances biomass production and promotes lateral root growth through an auxin dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592PubMedPubMedCentralCrossRefGoogle Scholar
  44. Cosme M, Ramireddy E, Franken P, Schmülling T, Wurst S (2016) Shoot- and root-borne cytokinin influences arbuscular mycorrhizal symbiosis. Mycorrhiza 26:709–720PubMedPubMedCentralCrossRefGoogle Scholar
  45. Cotxarrera L, Trillas-Gay MI, Steinberg C, Alabouvette C (2002) Use of sewage sludge compost and Trichoderma asperellum isolates to suppress fusarium wilt of tomato. Soil Biol Biochem 34:467–476CrossRefGoogle Scholar
  46. Courty PE, Smith P, Koegel S, Redeker D, Wipf D (2015) Inorganic nitrogen uptake and transport in beneficial plant root–microbe interactions. Crit Rev Plant Sci 34:4–16CrossRefGoogle Scholar
  47. Daguerre Y, Siegel K, Edel-Hermann V, Steinberg C (2014) Fungal proteins and genes associated with biocontrol mechanisms of soil-borne pathogens: a review. Fungal Biol Rev 28:97–125CrossRefGoogle Scholar
  48. Davies FT, Potter JR, Linderman RG (1993) Drought resistance of mycorrhizal pepper plants independent of leaf P-concentration – response in gas exchange and water relations. Physiol Plant 87:45–53CrossRefGoogle Scholar
  49. De Angeli A, Thomine S, Frachisse JM, Ephritikhine G, Gambale F, Barbier-Brygoo H (2007) Anion channels and transporters in plant cell membranes. FEBS Lett 581:2367–2374PubMedCrossRefGoogle Scholar
  50. De Hoog GS, Guarro J, Gene J, Figueras MJ (2000) Atlas of Clinical Fungi, vol 1, 2nd edn. Centraalbureau voor Schimmelcultures, UtrechtGoogle Scholar
  51. De Marco JL, Valadares-Inglis MC, Felix CR (2003) Production of hydrolytic enzymes by Trichoderma isolates with antagonistic activity against Crinipellis perniciosa, the causal agent of witches’ broom of cocoa. Braz J Microbiol 34:33–38CrossRefGoogle Scholar
  52. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430PubMedCrossRefGoogle Scholar
  53. Dehariya K, Shukla A, Sheikh IA, Vyas D (2015) Trichoderma and arbuscular mycorrhizal fungi based biocontrol of Fusarium udum Butler and their growth promotion effects on pigeon pea. J Agric Sci Technol 17:505–517Google Scholar
  54. Delaux PM, Varala K, Edger PP, Coruzzi GM, Pires JC, Ane JM (2014) Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genet 10:e1004487PubMedPubMedCentralCrossRefGoogle Scholar
  55. Denga JJ, Huanga WQ, Lia ZW, Lua DL, Zhangb Y, Luo XC (2018) Biocontrol activity of recombinant aspartic protease from Trichoderma harzianum against pathogenic fungi. Enzym Microb Technol 112:35–42CrossRefGoogle Scholar
  56. Diedhiou PM, Hallmann J, Oerke EC, Dehne HW (2003) Effects of arbuscular mycorrhizal fungi and non-pathogenic Fusarium oxysporum on Meloidogyne incognita infestation of tomato. Mycorrhiza 13:199–204PubMedCrossRefGoogle Scholar
  57. Djonovic S, Vittone G, Mendoza-Herrera A, Kenerley CM (2007) Enhanced biocontrol activity of Trichoderma virens transformants constitutively coexpressing β-1, 3-and β-1, 6-glucanase genes. Mol Plant Pathol 8:469–480PubMedCrossRefGoogle Scholar
  58. Dong Y, Zhu YG, Smith FA, Wang Y, Chen B (2008) Arbuscular mycorrhiza enhanced arsenic resistance of both white clover (Trifolium repens L.) and ryegrass (Lolium perenne L.) plants in an arsenic contaminated soil. Environ Pollut 15:174–181CrossRefGoogle Scholar
  59. Doni F, Isahak A, Zain CRCM, Ariffin SM, Mohamad WNW, Yusoff WMW (2014) Formulation of Trichoderma sp. SL2 inoculants using different carriers for soil treatment in rice seedling growth. Springerplus 3:1–5CrossRefGoogle Scholar
  60. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759PubMedCrossRefPubMedCentralGoogle Scholar
  61. Eke P, Chatue GC, Wakam LN, Kouipou RMT, Fokou PVT, Boyom FF (2016) Mycorrhiza consortia suppress the fusarium root rot (Fusarium solani f. sp. Phaseoli) in common bean (Phaseolus vulgaris L.). Biol Control 103:240–250CrossRefGoogle Scholar
  62. El-Hasan A, Walker F, Buchenauer H (2008) Trichoderma harzianum and its metabolite 6-Pentyl-alpha-pyrone suppress fusaric acid produced by Fusarium moniliforme. J Phytopathol 156:79–87CrossRefGoogle Scholar
  63. El-Hasan SA, Gowen SR, Pembroke B (2012) Use of Trichoderma hamatum for biocontrol of lentil vascular wilt disease: efficacy, mechanisms of interaction and future prospects. J Plant Protect Res 53:12–26CrossRefGoogle Scholar
  64. El-Komy MH, Saleh AA, Eranthodi A, Molan YY (2015) Characterization of novel Trichoderma asperellum isolates to select effective biocontrol agents against tomato Fusarium wilt. Plant Pathol J 31:50–60PubMedPubMedCentralCrossRefGoogle Scholar
  65. Elwakil MA, Baka ZA, Soliman HM, Sadek MS (2013) A modern tactic for reducing the biotic stress on cucumber plants caused by Fusarium oxysporum. Plant Pathol J 12:26–31CrossRefGoogle Scholar
  66. Escande AR, Laich FS, Pedraza MV (2002) Field testing of honey-bee dispersed Trichoderma spp. to manage sunflower head rot (Sclerotinia sclerotiorum). Plant Pathol 51:346–351CrossRefGoogle Scholar
  67. European Union (2009) Directive 2009/128/EC of the European Parliament and of the Council establishing a framework for Community action to achieve the sustainable use of pesticides. Off J Eur U. Accessed Aug 2018Google Scholar
  68. Eziashi EI, Uma NU, Adekunle AA, Airede CE (2006) Effect of metabolites produced by Trichoderma species against Ceratocystis paradoxa in culture medium. Afr J Biotechnol 5:703–706Google Scholar
  69. Ferrol N, Barea JM, Azcon-Aguilar C (2002) Mechanisms of nutrient transport across interfaces in arbuscular mycorrhizas. Plant Soil 244:231–237CrossRefGoogle Scholar
  70. Fiorilli V, Vannini C, Ortolani F, Garcia-Seco D, Chiapello M, Novero M, Domingo G, Terzi V, Morcia C, Bagnaresi P, Moulin L, Bracale M, Bonfante P (2018) Omics approaches revealed how arbuscular mycorrhizal symbiosis enhances yield and resistance to leaf pathogen in wheat. Sci Rep 8:1–18CrossRefGoogle Scholar
  71. Foo E, Ross JJ, Jones WT, Reid JB (2013) Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 111:769–779PubMedPubMedCentralCrossRefGoogle Scholar
  72. Fravel D, Olivain C, Alabouvette C (2003) Fusarium oxysporum and its biocontrol. New Phytol 157:493–502CrossRefGoogle Scholar
  73. Gadag AS, Krishnaraj PU (2017) Effect of Actinobacteria and Glomus fasiculatum against Fusarium oxysporum f. sp. lycopersici in Tomato Plant. Int J Curr Microbiol App Sci 6:488–498Google Scholar
  74. Gallou A, Mosquera HPL, Cranenbrouck S, Suaarez JP, Declerck S (2011) Mycorrhiza induced resistance in potato plantlets challenged by Phytophthora infestans. Physiol Mol Plant Pathol 76:20–26CrossRefGoogle Scholar
  75. Garcia-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386PubMedCrossRefPubMedCentralGoogle Scholar
  76. Garcia-Limones C, Hervas A, Navas-Cortes JA, Jimenez-Diaz RM, Tena M (2002) Induction of antioxidant enzyme system and other oxidative stress markers associated with compatible and incompatible interactions between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp. ciceris. Physiol Mol Plant Pathol 61:325–337CrossRefGoogle Scholar
  77. Gava CAT, Pinto JM (2016) Biocontrol of melon wilt caused by Fusarium oxysporum Schlect f. sp. melonis using seed treatment with Trichoderma spp. and liquid compost. Biol Control 97:13–20CrossRefGoogle Scholar
  78. Gianinazzi S, Vosatka M (2004) Inoculum of arbuscular mycorrhizal fungi for production systems: science meets business. Can J Bot 82:1264–1271CrossRefGoogle Scholar
  79. Giurgiu R, Dumitraș A, Morar G, Scheewe P, Schröder F (2018) A study on the biological control of Fusarium oxysporum using Trichoderma spp., on soil and rockwool substrates in controlled environment. Not Bot Horti Agrobot Cluj-Na 46:260–269CrossRefGoogle Scholar
  80. Grondona I, Hermosa R, Tejada M, Gomis MD, Mateos PF, Bridge PD, Monte E, Garcia-Acha I (1997) Physiological and biochemical characterization of Trichoderma harzianum, a biological control agent against soilborne fungal plant pathogens. Appl Environ Microbiol 63:3189–3198PubMedPubMedCentralGoogle Scholar
  81. Gutkind JS (1998) Cell growth control by G protein-coupled receptors: from signal transduction to signal integration. Oncogene 17:1331–1342PubMedCrossRefPubMedCentralGoogle Scholar
  82. Hage-Ahmed K, Krammer J, Steinkellner S (2013) The intercropping partner affects arbuscular mycorrhizal fungi and Fusarium oxysporum f. sp. Lycopersici interactions in tomato. Mycorrhiza 23:543–550PubMedPubMedCentralCrossRefGoogle Scholar
  83. Halder S, Ray MB (2006) Effect of VAM soil containing Glomus fasciculatum on growth of Withania somnifera Dun. Asian J Exp Sci 20:261–268Google Scholar
  84. Hanson LE (2000) Reduction of Verticillium wilt symptoms in cotton following seed treatment with Trichoderma virens. J Cotton Sci 4:224–231Google Scholar
  85. Hao Z, Christie P, Qin L, Wang C, Li X (2005) Control of Fusarium Wilt of cucumber seedlings by inoculation with an arbuscular mycorrhical fungus. J Plant Nutr 28:1961–1974CrossRefGoogle Scholar
  86. Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190–194CrossRefGoogle Scholar
  87. Harman GE, Shoresh M (2007) The mechanisms and applications of symbiotic opportunistic plant symbiont. In: Vurro M, Gressel J (eds) Novel biotechnologies for biocontrol agent enhancement and management. NATO security through science series. Springer, DordrechtGoogle Scholar
  88. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2(1):43–56PubMedCrossRefPubMedCentralGoogle Scholar
  89. Harrier LA, Watson CA (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. Pest Manag Sci 60:149–157PubMedCrossRefPubMedCentralGoogle Scholar
  90. Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 8:101–110CrossRefGoogle Scholar
  91. Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25CrossRefGoogle Scholar
  92. Herrera-Medina MJ, Tamayo MI, Vierheilig H, Ocampo JA, Garcia-Garrido JM (2008) The jasmonic acid signalling pathway restricts the development of the arbuscular mycorrhizal association in tomato. J Plant Growth Regul 27:221–230CrossRefGoogle Scholar
  93. Hinsinger P, Betencourt E, Bernard L, Brauman A, Plassard C, Shen J, Tang X, Zhang F (2011) P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol 156:1078–1086PubMedPubMedCentralCrossRefGoogle Scholar
  94. Hirpara DG, Gajera HP (2018) Molecular heterozygosity and genetic exploitations of Trichoderma inter-fusants enhancing tolerance to fungicides and mycoparasitism against Sclerotium rolfsii Sacc. Infect Genet Evol 66:26–36PubMedCrossRefPubMedCentralGoogle Scholar
  95. Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10PubMedCrossRefPubMedCentralGoogle Scholar
  96. Howell CR (2006) Understanding the mechanisms employed by Trichoderma virens to effect biological control of cotton diseases. Phytopathology 96:178–180CrossRefGoogle Scholar
  97. Howell CR, Hanson EL, Stipanovic RD, Puckhaber LS (2000) Induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. Phytopathology 90:248–252PubMedCrossRefPubMedCentralGoogle Scholar
  98. Huang C, Roberts PD, Datnoff LE (2011) Silicon suppresses Fusarium crown and root rot of tomato. J Phytopathol 159:546–554CrossRefGoogle Scholar
  99. Jaiti F, Meddich A, El-Hadrami I (2008) Effectiveness of arbuscular mycorrhizal fungi in the protection of date palm (Phoenix dactylifera L.) against bayoud disease. Physiol Mol Plant Pathol 71:166–173CrossRefGoogle Scholar
  100. Jakobsen I (1999) Transport of phosphorus and carbon in arbuscular mycorrhizas. In: Varma A, Hock B (eds) Mycorrhiza. Springer, BerlinGoogle Scholar
  101. Jayalakshmi SK, Raju S, Usha Rani S, Benagi VI, Sreeramulu K (2009) Trichoderma harzianum L1 as a potential source for lytic enzymes and elicitor of defense responses in chickpea (Cicer arietinum L.) against wilt disease caused by Fusarium oxysporum f. sp. ciceri. Aust J Crop Sci 3:44–52Google Scholar
  102. Jimenez C, Ricardo D (2017) Soybean root rot caused by Fusarium oxysporum and Fusarium graminearum: interactions with biotic and abiotic factors. Graduate theses and dissertations. PhD dissertation, Iowa State University, Ames, IAGoogle Scholar
  103. Johri AK, Oelmuller R, Dua M, Yadav V, Kumar M, Tuteja N, Varma A, Bonfante P, Persson BL, Stroud RM (2015) Fungal association and utilization of phosphate by plants: success, limitations, and future prospects. Front Microbiol 6:1–13CrossRefGoogle Scholar
  104. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  105. Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664PubMedCrossRefGoogle Scholar
  106. Kamala T, Indira S (2011) Evaluation of indigenous Trichoderma isolates from Manipur as biocontrol agent against Pythium aphanidermatum on common beans. 3 Biotech 1:217–225PubMedPubMedCentralCrossRefGoogle Scholar
  107. Kazan K (2013) Auxin and the integration of environmental signals into plant root development. Ann Bot 112:1655–1665PubMedPubMedCentralCrossRefGoogle Scholar
  108. Keymer A, Gutjahr C (2018) Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Curr Opin Plant Biol 44:137–144PubMedCrossRefGoogle Scholar
  109. Khan MH, Meghvansi MK, Panwar V, Gogoi HK, Singh L (2010) Arbuscular mycorrhizal fungi-induced signalling in plant defence against phytopathogens. J Phytol 2:53–69Google Scholar
  110. Kieber JJ, Schaller GE (2014) Cytokinins. In: The arabidopsis book. The American Society of Plant Biologists, p e0168Google Scholar
  111. Kiriga AW, Haukelandb S, Kariukia GM, Coynec DL, Beek NV (2018) Effect of Trichoderma spp. and Purpureocillium lilacinum on Meloidogyne javanica in commercial pineapple production in Kenya. Biol Control 119:27–32CrossRefGoogle Scholar
  112. Komy MHE, Saleh AA, Eranthodi A, Molan YY (2015) Characterization of novel Trichoderma asperellum isolates to select effective biocontrol agents against tomato Fusarium wilt. Plant Pathol J 31:50–60PubMedCrossRefGoogle Scholar
  113. Kredics L, Antal Z, Szekeres A, Hatvani L, Manczinger L, Vágvölgyi C, Nagy E (2005) Extracellular proteases of Trichoderma species: a review. Acta Microbiol Immunol Hung 52:169–184PubMedCrossRefGoogle Scholar
  114. Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780–790PubMedCrossRefGoogle Scholar
  115. Kumar V, Shahid M, Singh A, Srivastava M, Mishra A, Srivastava YK, Pandey S, Shrarma A (2014) Effect of biopriming with biocontrol agents Trichoderma harzianum (Th.Azad) and Trichoderma viride (01pp) on chickpea Genotype (Radhey). J Plant Pathol Microb 5:1–4Google Scholar
  116. Lambais MR (2006) Unraveling the signaling and signal transduction mechanisms controlling arbuscular mycorrhiza development. Sci Agric 63:405–413CrossRefGoogle Scholar
  117. Li Y, Yanagi A, Miyawaki Y, Okada T, Matsubara Y (2010) Disease tolerance and changes in antioxidative abilities in mycorrhizal strawberry plants. J Jpn Soc Hortic Sci 79:174–178CrossRefGoogle Scholar
  118. Li Q-R, Tan P, Yiang Y-L, Hyde KD, Mckenzie EHC, Bahkali AH, Kang C, Wang Y (2013) A novel Trichoderma species isolated from soil in Guizhou, T. guizhouense. Mycol Prog 12:167–172CrossRefGoogle Scholar
  119. Li YT, Hwang SG, Huang YM, Huang CH (2018) Effects of Trichoderma asperellum on nutrient uptake and Fusarium wilt of tomato. Crop Prot 110:275–282CrossRefGoogle Scholar
  120. Li-Jun M, Geiser DM, Proctor RH, Rooney AP, O’Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K (2013) Fusarium Pathogenomics. Annu Rev Microbiol 67:399–416CrossRefGoogle Scholar
  121. Lima FB, Felix C, Osorio N, Alves A, Vitorino R, Domingues P, Correia A, RTdS R, Esteves AC (2016) Secretome analysis of Trichoderma atroviride T17 biocontrol of Guignardia citricarpa. Biol Control 99:38–46CrossRefGoogle Scholar
  122. 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 50:529–544PubMedCrossRefGoogle Scholar
  123. Lopez-Bucio J, Pelagio-Flores R, Herrera-Estrella A (2015) Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Sci Hortic 196:109–123CrossRefGoogle Scholar
  124. Lopez-Raez JA, Flors V, Garcia JM, Pozo MJ (2010) AM symbiosis alters phenolic acid content in tomato roots. Plant Signal Behav 5:1–3CrossRefGoogle Scholar
  125. Ludwig-Muller J (2010) Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 169–190CrossRefGoogle Scholar
  126. Ludwig-Muller J, Guther M (2007) Auxins as signals in arbuscular mycorrhiza formation. Plant Signal Behav 2:194–196PubMedPubMedCentralCrossRefGoogle Scholar
  127. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee YH, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park SY, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, Sykes S, Schwartz DC, Turgeon BG, Wapinski I, Yoder O, Young S, Zeng Q, Zhou S, Galagan J, Cuomo CA, Kistler HC, Rep M (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373PubMedPubMedCentralCrossRefGoogle Scholar
  128. Macho AP, Zipfel C (2014) Plant PRRs and the activation of innate immune signaling. Mol Cell 54:263–273PubMedCrossRefGoogle Scholar
  129. Mahajan K, Sharma JK, Dhage A (2018) Evaluation of Trichoderma sp. against Fusarium wilt of chickpea caused by Fusarium oxysporum f. sp. ciceris under in vitro condition. Int J Curr Microbiol Appl Sci 7:595–599Google Scholar
  130. Martinez-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 seedling nurseries. J Sci Food Agric 89:1843–1850CrossRefGoogle Scholar
  131. Marzano M, Gallo A, Altomare C (2013) Improvement of biocontrol efficacy of Trichoderma harzianum vs. Fusarium oxysporum f. sp. lycopersici through UV-induced tolerance to fusaric acid. Biol Control 67:397–408CrossRefGoogle Scholar
  132. Mathur N, Vyas A (1995) Influence of VAM on net photosynthesis and transpiration of Ziziphus mauritiana. J Plant Physiol 147:328–330CrossRefGoogle Scholar
  133. Matsubara Y, Ohba N, Fukui H (2001) Effect of arbuscular mycorrhizal fungus infection on the incidence of Fusarium root rot in asparagus seedlings. J Jpn Soc Hortic Sci 70:202–206CrossRefGoogle Scholar
  134. Matsubara Y, Hirano I, Sassa D, Koshikawa K (2004) Increased tolerance to fusarium wilt in mycorrhizal strawberry plants raised by capillary watering methods. Environ Contam Biol 42:185–191CrossRefGoogle Scholar
  135. Mayer AM (2006) Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67:2318–2331PubMedCrossRefPubMedCentralGoogle Scholar
  136. Meixner C, Ludwig-Muller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the super nodulating soybean mutant nts1007. Planta 222:709–715PubMedCrossRefPubMedCentralGoogle Scholar
  137. Mendoza-Mendoza A, Zaid R, Lawry R, Hermosa R, Monte E, Horwitz BA, Mukherjee PK (2018) Molecular dialogues between Trichoderma and roots: role of the fungal secretome. Fungal Biol Rev 32:62–85CrossRefGoogle Scholar
  138. Mir GH, Devi LS, Ahamd S, Kumar VM, Williams P (2011) Antagonistic potential of native isolates of Trichoderma viride on corm rot pathogen complex of saffron (Crocus sativas) in Kashmir. Plant Pathol J 10:73–78CrossRefGoogle Scholar
  139. Mishra V, Ellouze W, Howard RJ (2018) Utility of arbuscular mycorrhizal fungi for improved production and disease mitigation in organic and hydroponic greenhouse crops. J Hortic 5:1–10CrossRefGoogle Scholar
  140. Mohammadi M, Kazemi H (2002) Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Sci 162:491–498CrossRefGoogle Scholar
  141. Mohandas S, Manjula R, Rawal RD, Lakshmikantha HC, Saikat C, Ramachandra YL (2010) Evaluation of arbuscular mycorrhiza and other biocontrol agents in managing Fusarium oxysporum f. sp. cubense infection in banana cv. Neypoovan. Biocontrol Sci Technol 20:165–181CrossRefGoogle Scholar
  142. Monteiro VN, Silva RN, Steindorf AS, Costa FT, Noronha EF, Ricart CAO, Sousa MV, Vainstein MH, Ulhoa CJ (2010) New insights in Trichoderma harzianum antagonism of fungal plant pathogens by secreted protein analysis. Curr Microbiol 61:298–305PubMedCrossRefGoogle Scholar
  143. Morkunas I, Gemerek J (2007) The possible involvement of peroxidase in defense of yellow lupin embryo axes against Fusarium oxysporum. J Plant Physiol 164:497–506CrossRefGoogle Scholar
  144. Mostert D, Molina AB, Daniells J, Fourie G, Hermanto C, Chao C-P, Fabregar E, Sinohin VG, Masdek N, Thangavelu R, Li C, Yi G, Mostert L, Viljoen A (2017) The distribution and host range of the banana Fusarium wilt fungus, Fusarium oxysporum f. sp. cubense, in Asia. PLoS One 12:e0181630PubMedPubMedCentralCrossRefGoogle Scholar
  145. Mukherjee PK (1997) Trichoderma sp. as a microbial suppressive agent of Sclerotium rolfsii on vegetables. World J Microbiol Biotechnol 13:497–499CrossRefGoogle Scholar
  146. Mukherjee M, Mukherjee PK, Horwitz BA, Zachow C, Berg G, Zeilinger S (2012) Trichoderma–plant–pathogen interactions: advances in genetics of biological control. Indian J Microbiol 52:522–529PubMedPubMedCentralCrossRefGoogle Scholar
  147. Mukherjee PK, Horwitz BA, Singh US, Mukherjee M, Schmoll M (2013a) Trichoderma in agriculture, industry and medicine: an overview. In: Mukherjee PK, Horwitz BA, Singh US, Mukherjee M, Schmoll M (eds) Trichoderma: biology and applications. CABI, Nosworthy, Way, Wallingford, OX, pp 1–9CrossRefGoogle Scholar
  148. Mukherjee PK, Horwitz BA, Herrera-Estrella A, Schmoll M, Kenerley CM (2013b) Trichoderma research in the genome era. Annu Rev Phytopathol 51:105–129PubMedCrossRefGoogle Scholar
  149. Nair A, Kolet SP, Thulsiram HV, Bhargava S (2015) Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. Plant Biol (Stuttg) 17:625–631CrossRefGoogle Scholar
  150. Nelson BD, Hansen JM, Windels CE, Helms TC (1997) Reaction of soybean cultivars to isolates of Fusarium solani from the Red River Valley. Plant Dis 81:664–668PubMedCrossRefGoogle Scholar
  151. Nucci M, Anaissie E (2007) Fusarium infections in immunocompromised patients. Clin Microbiol Rev 20:695–704PubMedPubMedCentralCrossRefGoogle Scholar
  152. O’Donnell K, Sutton DA, Fothergill A, McCarthy D, Rinaldi MG, Brandt ME, Zhang N, Geiser DM (2008) Molecular phylogenetic diversity, multilocus haplotype nomenclature, and in vitro antifungal resistance within the Fusarium solani species complex. J Clin Microbiol 46:2477–2490PubMedPubMedCentralCrossRefGoogle Scholar
  153. Omomowo IO, Fadiji AE, Omomowo OI (2018) Assessment of bio-efficacy of Glomus versiforme and Trichoderma harzianum in inhibiting powdery mildew disease and enhancing the growth of cowpea. Ann Agric Sci 63:9–17CrossRefGoogle Scholar
  154. Oyetunji OJ, Salami AO (2011) Study on the control of Fusarium wilts in the stems of mycorrhizal and trichodermal inoculated pepper (Capsicum annum L.). J Appl Biosci 45:3071–3080Google Scholar
  155. Ozgonen H, Bicici M, Erkilic A (1999) The effect of salicylic acid and endomycorrhizal fungus G. intraradices on plant development of tomato and fusarium wilt caused by Fusarium oxysporum f. sp. lycopersici. Turk J Agric For 25:25–29Google Scholar
  156. Patole SP, Dhore SB, Pradhan RS, Shankara K (2017) In vitro evaluation of Trichoderma viride and Trichoderma harzianum against Fusarium wilt of Chickpea. Int J Pure App Biosci 5:460–464CrossRefGoogle Scholar
  157. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316CrossRefGoogle Scholar
  158. Pineda A, Zheng SJ, van Loon JJ, Pieterse CM, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514PubMedCrossRefPubMedCentralGoogle Scholar
  159. Ponce de Leon I, Montesano M (2013) Activation of defense mechanisms against pathogens in mosses and flowering plants. Int J Mol Sci 14:3178–3200PubMedCrossRefPubMedCentralGoogle Scholar
  160. Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398PubMedCrossRefPubMedCentralGoogle Scholar
  161. Pozo MJ, Lopez-Raez JA, Azcon-Aguilar C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205:1431–1436PubMedCrossRefPubMedCentralGoogle Scholar
  162. Prasad R, Bhola D, Akdi K, Cruz C, Sairam KVSS, Tuteja N, Varma A (2017) Introduction to mycorrhiza: historical development. In: Varma A, Prasad R, Tuteja N (eds) Mycorrhiza. Springer International Publishing AG, Cham, pp 1–7Google Scholar
  163. Probst C, Bandyopadhyay R, Price LE, Cotty PJ (2011) Identification of atoxigenic Aspergillus flavus isolates to reduce aflatoxin contamination of maize in Kenya. Plant Dis 95:212–218PubMedCrossRefPubMedCentralGoogle Scholar
  164. Pusztahelyi T, Holb IJ, Pocsi I (2017) Plant-fungal interactions: special secondary metabolites of the biotrophic, necrotrophic, and other specific interactions. In: Merillon JM, Ramawat KG (eds) Fungal metabolites. Springer International Publishing, Cham, pp 133–190CrossRefGoogle Scholar
  165. Qualhato TF, Lopes FAC, Steindorff AS, Brandão RS, Jesuino RSA, Ulhoa CJ (2013) Mycoparasitism studies of Trichoderma species against three phytopathogenic fungi: evaluation of antagonism and hydrolytic enzyme production. Biotechnol Lett 35(9):1461–1468PubMedCrossRefGoogle Scholar
  166. Rahman SFSA, Singh E, Pieterse CMJ, Schenk PM (2018) Emerging microbial biocontrol strategies for plant pathogens. Plant Sci 267:102–111CrossRefGoogle Scholar
  167. Raman N, Gnanaguru M, Srinivasan V (2001) Biological control of Fusarium wilt of tomato by VA mycorrhizal fungus Glomus fasciculatum. Bulletin-OILB-SROP 24:33–36Google Scholar
  168. Ranf S (2017) Sensing of molecular patterns through cell surface immune receptors. Curr Opin Plant Biol 38:68–77PubMedCrossRefPubMedCentralGoogle Scholar
  169. Rao GS, Reddy NNR, Surekha C (2015) Induction of plant systemic resistance in legumes Cajanus cajan, Vigna radiata, Vigna mungo against plant pathogens Fusarium oxysporum and Alternaria alternata – a Trichoderma viride mediated reprogramming of plant defense mechanism. Int J Recent Sci Res 6:4270–4280Google Scholar
  170. Ren L, Lou Y, Sakamoto K, Inubushi K, Amemiya Y, Shen Q, Xu G (2010) Effects of Arbuscular mycorrhizal colonization on microbial community in rhizosphere soil and Fusarium wilt disease in tomato. Commun Soil Sci Plant Anal 41:1399–1410CrossRefGoogle Scholar
  171. Ren CG, Kong CC, Xie ZH (2018) Role of abscisic acid in strigolactone induced salt stress tolerance in arbuscular mycorrhizal Sesbania cannabina seedlings. BMC Plant Biol 18:74PubMedPubMedCentralCrossRefGoogle Scholar
  172. Rey M, Delgado J, Rincon A, Carmen L, Benitez T, Perez E (2000) Improvement of Trichoderma strains for biocontrol. Rev Iberoam Micol 17:31–36Google Scholar
  173. Reynolds HL, Hartley AE, Vogelsang KM, Bever JD, Schultz PA (2005) Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. New Phytol 167:869–880PubMedCrossRefPubMedCentralGoogle Scholar
  174. Rifai MA (1969) A revision of genus Trichoderma. Commonow Mycol Inst Mycol:116–156Google Scholar
  175. Robinson-Boyer L, Grzyb I, Jeffries P (2009) Shifting the balance from qualitative to quantitative analysis of arbuscular mycorrhizal communities in field soils. Fungal Ecol 2:1–9CrossRefGoogle Scholar
  176. Roco A, Perez LM (2001) In vitro biocontrol activity of Trichoderma harzianum on Alternaria alternata in the presence of growth regulators. Electron J Biotechnol 4:68–73Google Scholar
  177. Ruelas C, Tiznado-Hernandez ME, Sanchez-Estrada A, Robles-Burgueno MR, Troncoso-Rojas R (2006) Changes in phenolic acid content during Alternaria alternata infection in tomato fruit. J Phytopathol 154:236–244CrossRefGoogle Scholar
  178. 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
  179. Samolski I, Rincon AM, Pinzon LM, Viterbo A, Monte E (2012) The qid74 gene from Trichoderma harzianum has a role in root architecture and plant bio-fertilization. Microbiology 158:129–138PubMedCrossRefPubMedCentralGoogle Scholar
  180. Samuels GJ (1996) Trichoderma: a review of biology and systematic of the genus. Mycol Res 100:923–935CrossRefGoogle Scholar
  181. Saravanakumar K, Yu C, Dou K, Wang M, Li Y, Chen J (2016) Synergistic effect of Trichoderma-derived antifungal metabolites and cell wall degrading enzymes on enhanced biocontrol of Fusarium oxysporum f. sp. Cucumerinum. Biol Control 94:37–46CrossRefGoogle Scholar
  182. Saravanakumar K, Dou K, Lu Z, Wang X, Li Y, Chen J (2018) Enhanced biocontrol activity of cellulase from Trichoderma harzianum against Fusarium graminearum through activation of defense-related genes in maize. Physiol Mol Plant Pathol 103:130–136CrossRefGoogle Scholar
  183. Saremi H, Saremi H (2013) Isolation of the most common Fusarium species and the effect of soil solarisation on main pathogenic species in different climatic zones of Iran. Eur J Plant Pathol 137:585–596CrossRefGoogle Scholar
  184. Sawers RJH, Gutjahr C, Paszkowski U (2007) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13:93–97CrossRefGoogle Scholar
  185. Scheffknecht S, Mammerler R, Steinkellner S, Vierheilig H (2006) Root exudates of mycorrhizal tomato plants exhibit a different effect on microconidia germination of Fusarium oxysporum f. sp. lycopersici than root exudates from non-mycorrhizal tomato plants. Mycorrhiza 16:365–370PubMedCrossRefPubMedCentralGoogle Scholar
  186. Scheffknecht S, St-Arnaud M, Khaosaad T, Steinkellner S, Vierheilig H (2007) An altered root exudation pattern through mycorrhization affecting microconidia germination of the highly specialized tomato pathogen Fusarium oxysporum f. sp. lycopersici (Fol) is not tomato specific but also occurs in Fol non-host plants. Can J Bot 85:347–351CrossRefGoogle Scholar
  187. Schmitt FJ, Renger G, Friedrich T, Kreslavksi VD, Zharmukhadmedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochim Biophys Acta 1837:835–848PubMedCrossRefPubMedCentralGoogle Scholar
  188. Schmitz AM, Harrison MJ (2014) Signaling events during initiation of arbuscular mycorrhizal symbiosis. J Integr Plant Biol 56:250–261PubMedCrossRefPubMedCentralGoogle Scholar
  189. Schmoll M (2008) The information highways of a biotechnological workhorse-signal transduction in Hypocrea jecorina. BMC Genomics 9:430PubMedPubMedCentralCrossRefGoogle Scholar
  190. Score AJ, Palfreyman JW (1994) Biological control of the dry rot fungus Serpula lacrymans by Trichoderma species: the effects of complex and synthetic media on interaction and hyphal extension rates. Int Biodeterior Biodegrad 33:115–128CrossRefGoogle Scholar
  191. Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signaling: reactive oxygen species at the cross-road. Front Plant Sci 7:1–21CrossRefGoogle Scholar
  192. Shanmugaiah V, Balasubramanian N, Gomathinayagam S, Manoharan PT, Rajendran A (2009) Effect of single application of Trichoderma viride and Pseudomonas fluorescens on growth promotion in cotton plants. Afr J Agric Res 4:1220–1225Google Scholar
  193. Sharma R, Bhat S (2012) Molecular screening of the presence of ech33 from Trichoderma isolate of India. Wudpecker J Agric Res 1:429–432Google Scholar
  194. Sharma A, Rathour R, Plaha P, Katoch V, Khalsa GS, Patial V, Singh Y, Pathania NK (2010) Induction of Fusarium wilt (Fusarium oxysporum f. sp. pisi) resistance in garden pea using induced mutagenesis and in vitro selection techniques. Euphytica 173:345–356CrossRefGoogle Scholar
  195. Sharma P, Ponnusamy VK, Ramesh R, Saravanan K, Deep S, Sharma M, Mahesh S, Dinesh S (2011) Biocontrol genes from Trichoderma species: a review. Afr J Biotechnol 10:19898–19907Google Scholar
  196. Sharma V, Salwan R, Sharma PN (2017) The comparative mechanistic aspects of Trichoderma and probiotics: scope for future research. Physiol Mol Plant Pathol 100:84–96CrossRefGoogle Scholar
  197. Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296PubMedCrossRefPubMedCentralGoogle Scholar
  198. Sheng M, Tang M, Zhang F, Huang Y (2011) Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21:423–430PubMedCrossRefPubMedCentralGoogle Scholar
  199. Sikes BA (2010) When do arbuscular mycorrhizal fungi protect plant roots from pathogens? Plant Signal Behav 5:763–765PubMedPubMedCentralCrossRefGoogle Scholar
  200. Singh HB, Singh BN, Singh SP, Singh SR, Sarma BK (2009) Biological control of plant diseases: current status and future prospects. In: Johri JK (ed) Recent advances in biopesticides: biotechnological applications. New India Publishing Agency, New Delhi, p 322Google Scholar
  201. Singh PK, Mishra M, Vyas D (2010) Effect of root exudates of mycorrhizal tomato plants on microconidia germination of Fusarium oxysporum f. sp. lycopersici than root exudates from non-mycorrhizal tomato plants. Arch Phytopathol Plant Protect 43:1495–1503CrossRefGoogle Scholar
  202. Singh R, Maurya S, Upadhyay RS (2016) The improvement of competitive saprophytic capabilities of Trichoderma species through the use of chemical mutagens. Braz J Microbiol 47:10–17CrossRefGoogle Scholar
  203. Smith SE, Read DJ (2002) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  204. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, San Diego, CAGoogle Scholar
  205. Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:1–13Google Scholar
  206. Suarez MB, Vizcaíno JA, Llobell A, Monte E (2007) Characterization of genes encoding novel peptidases in the biocontrol fungus Trichoderma harzianum CECT 2413 using the TrichoEST functional genomics approach. Curr Genet 51:331–342PubMedCrossRefGoogle Scholar
  207. Sun Z, Song J, Xin X, Xie X, Zhao B (2018) Arbuscular mycorrhizal fungal 14-3-3 proteins are involved in arbuscule formation and responses to abiotic stresses during AM symbiosis. Front Microbiol 9:1–17CrossRefGoogle Scholar
  208. Suzuki N, Bassil E, Hamilton JS, Inupakutika MA, Zandalinas SI, Tripathy D, Luo Y, Dion E, Fukui G, Kumazaki A, Nakano R, Rivero RM, Verbeck GF, Azad RK, Blumwald E, Mittler R (2016) ABA is required for plant acclimation to a combination of salt and heat stress. PLoS One 11:e0147625PubMedPubMedCentralCrossRefGoogle Scholar
  209. Svenningsen NB, Watts-Williams SJ, Joner EJ, Battini F, Efthymiou A, Cruz-Paredes C, Nybroe O, Jakobsen I (2018) Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME J 12:1296–1307PubMedPubMedCentralCrossRefGoogle Scholar
  210. Tawaraya K, Turjaman M, Ekamawanti HA (2007) Effect of arbuscular mycorrhiza colonization on nitrogen and phosphorus uptake and growth of Aloe vera L. HortSci 42:1737–1739CrossRefGoogle Scholar
  211. Tayal P, Kapoor R, Bhatnagar AK (2011) Functional synergism among Glomus fasciculatum, Trichoderma viride and Pseudomonas fluorescens on Fusarium wilt in tomato. J Plant Pathol 93:745–750Google Scholar
  212. Thakker JN, Patel S, Dhandhukia PC (2013) Induction of defense-related enzymes in banana plants: effect of live and dead pathogenic strain of Fusarium oxysporum f. sp. cubense. ISRN Biotechnol. doi: Google Scholar
  213. Tian C, Kasiborski B, Koul R, Lammers PJ, Bucking H, Shachar-Hill Y (2010) Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux. Plant Physiol 153:1175–1187PubMedPubMedCentralCrossRefGoogle Scholar
  214. Toghueo RMK, Eke P, Zabalgogeazcoa I, de Aldana BRV, Nana LW, Boyom FF (2018) Bio control and growth enhancement potential of two endophytic Trichoderma spp. from Terminalia catappa against the causative agent of Common Bean Root Rot (Fusarium solani). Biol Control 96:8–20CrossRefGoogle Scholar
  215. Trepanier M, Becard G, Moutoglis P, Willemot C, Gagne S, Avis TJ, Rioux JA (2005) Dependence of arbuscular-mycorrhizal fungi on their plant host for palmitic acid synthesis. Appl Environ Microbiol 71:5341–5347PubMedPubMedCentralCrossRefGoogle Scholar
  216. Troian RF, Steindorff AS, Ramada MHS, Arruda W, Ulhoa CJ (2014) Mycoparasitism studies of Trichoderma harzianum against Sclerotinia sclerotiorum: evaluation of antagonism and expression of cell wall-degrading enzymes genes. Biotechnol Lett 36:2095–2101PubMedCrossRefGoogle Scholar
  217. Utkhede R (2006) Increased growth and yield of hydroponically grown greenhouse tomato plants inoculated with arbuscular mycorrhizal fungi and Fusarium oxysporum f. sp. radicis-lycopersici. BioControl 51:393–400CrossRefGoogle Scholar
  218. van Loon LC (1997) Induced resistance in plants and the role of pathogenesis-related proteins. Eur J Plant Pathol 103:753–765CrossRefGoogle Scholar
  219. Van Wees SCM, der Ent SV, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448PubMedCrossRefGoogle Scholar
  220. Veerabhadraswamy AL, Garampalli RH (2011) Effect of arbuscular mycorrhizal fungi in the management of black bundle disease of maize caused by Cephalosporium acremonium. Sci Res Repot 1:96–100Google Scholar
  221. Velivelli SL, Lojan P, Cranenbrouck S, de Boulois HD, Suarez JP, Declerck S, Franco J, Prestwich BD (2015) The induction of Ethylene response factor 3 (ERF3) in potato as a result of co-inoculation with Pseudomonas sp. R41805 and Rhizophagus irregularis MUCL 41833-a possible role in plant defense. Plant Signal Behav 10:e988076PubMedPubMedCentralCrossRefGoogle Scholar
  222. Veresoglou SF, Chen B, Rillig MC (2012) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol Biochem 46:53–62CrossRefGoogle Scholar
  223. Verma M, Brar S, Tyagi R, Surampalli R, Valero J (2007) Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J 37:1–20CrossRefGoogle Scholar
  224. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma-plant-pathogen interactions. Soil Biol Biochem 40:1–10CrossRefGoogle Scholar
  225. Vinodkumar S, Indumathi T, Nakkeeran S (2017) Trichoderma asperellum (NVTA2) as a potential antagonist for the management of stem rot in carnation under protected cultivation. Biol Control 113:58–64CrossRefGoogle Scholar
  226. Viterbo A, Wiest A, Brotman Y, Chet I, Kenerley C (2007) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746PubMedCrossRefGoogle Scholar
  227. Vos CM, Yang Y, De Coninck B, Cammue BPA (2014) Fungal (-like) biocontrol organisms in tomato disease control. Biol Control 74:65–81CrossRefGoogle Scholar
  228. Waghmare SJ, Kurundkar BP (2011) Efficacy of local isolates of Trichoderma spp against Fusarium oxysporum sp. carthami causing wilt of safflower. Adv Plant Sci 24:37–38Google Scholar
  229. Waghunde RR, Shelake RM, Sabalpara AN (2016) Trichoderma: a significant fungus for agriculture and environment. Afr J Agric Res 11:1952–1965Google Scholar
  230. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363PubMedCrossRefGoogle Scholar
  231. Wang C, Li X, Song F (2012) Protecting cucumber from Fusarium wilt with arbuscular mycorrhizal fungi. Commun Soil Sci Plant Anal 43:2851–2864CrossRefGoogle Scholar
  232. Wang W, Shi J, Xie Q, Jiang Y, Yu N, Wang E (2017) Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Mol Plant 10:1147–1158CrossRefPubMedPubMedCentralGoogle Scholar
  233. Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291–322PubMedPubMedCentralCrossRefGoogle Scholar
  234. Watts-Williams SJ, Cavagnaro TR (2018) Arbuscular mycorrhizal fungi increase grain zinc concentration and modify the expression of root ZIP transporter genes in a modern barley (Hordeum vulgare) cultivar. Plant Sci 274:163–170PubMedCrossRefGoogle Scholar
  235. Weindling R (1932) Trichoderma lignorum as a parasitic of other fungi. Phytopathology 22:837–845Google Scholar
  236. Willmann A, Thomfohrde S, Haensch R, Nehls U (2014) The poplar NRT2 gene family of high affinity nitrate importers: impact of nitrogen nutrition and ecto-mycorrhiza formation. Environ Exp Bot 108:79–88CrossRefGoogle Scholar
  237. Wu QS, Srivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic (Amst) 164:77–87CrossRefGoogle Scholar
  238. Wuyts N, Swennen R, De Waele D (2006) Effects of plant phenylpropanoid pathway products and selected terpenoids and alkaloids on the behaviour of the plant-parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne incognita. Nematology 8:89–101CrossRefGoogle Scholar
  239. Xu M, Dong J, Wang H, Huang L (2009) Complementary action of jasmonic acid on salicylic acid in mediating fungal elicitor-induced flavonol glycoside accumulation of Ginkgo biloba cells. Plant Cell Environ 32:960–967PubMedCrossRefGoogle Scholar
  240. Xue AG, Guo W, Chen Y, Siddiqui I, Marchand G, Liu J, Ren C (2017) Effect of seed treatment with novel strains of Trichoderma spp. on establishment and yield of spring wheat. Crop Prot 96:97–102CrossRefGoogle Scholar
  241. Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150PubMedCrossRefGoogle Scholar
  242. Zeilinger S, Gruber S, Bansal R, Mukherjee PK (2016) Secondary metabolism in Trichoderma-chemistry meets genomics. Fungal Biol Rev 30:74–90CrossRefGoogle Scholar
  243. Zeriouh W, Nani A, Belarbi M, Dumont A, de Rosny C, Aboura I, Ghanemi FZ, Murtaza B, Patoli D, Thomas C, Apetoh L, Rebe C, Delmas D, Khan NA, Ghiringhelli F, Rialland M, Hichami A (2017) Phenolic extract from oleaster (Olea europaea var. Sylvestris) leaves reduces colon cancer growth and induces caspase-dependent apoptosis in colon cancer cells via the mitochondrial apoptotic pathway. PLoS One 12:e0170823PubMedPubMedCentralCrossRefGoogle Scholar
  244. Zimmermann J, Musyoki MK, Cadisch G, Rasche F (2016) Biocontrol agent Fusarium oxysporum f. sp. strigae has no adverse effect on indigenous total fungal communities and specific AMF taxa in contrasting maize rhizospheres. Fungal Ecol 23:1–10PubMedPubMedCentralCrossRefGoogle Scholar
  245. Zorb C, Geilfus CM, Mühling KH, Ludwig-Muller J (2013) The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J Plant Physiol 170:220–224PubMedCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of BotanySavitribai Phule Pune UniversityPuneIndia
  2. 2.Division of Biochemistry, Department of ChemistrySavitribai Phule Pune UniversityPuneIndia

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