Skip to main content
SpringerLink
Log in

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

  • Chapter
  • First Online:
Plant Microbe Interface

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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 166:268–281

    Article  CAS  PubMed  Google Scholar 

  • Abhiram P, Masih H (2018) In vitro Antagonism of Trichoderma viride against Fusarium oxysporum strains. J Pharmacogn Phytochem 7:2816–2819

    CAS  Google Scholar 

  • 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 158:475–482

    Article  CAS  PubMed  Google Scholar 

  • Agrios GN (1988) Plant pathology, 3rd edn. Academic, New York, p 803

    Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  CAS  PubMed  Google Scholar 

  • 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 153:544–550

    Article  Google Scholar 

  • Alabouvette C, Lemanceau P, Steinberg C (1993) Recent advances in the biological control of Fusarium wilts. Pestic Sci 37:365–373

    Article  Google Scholar 

  • 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 184:529–544

    Article  CAS  PubMed  Google Scholar 

  • 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 23:288–292

    Article  PubMed  Google Scholar 

  • Al-Hmoud G, Al-Momany A (2015) Effect of four mycorrhizal products on Fusarium root rot on different vegetable crops. J Plant Pathol Microb 6:255

    Google Scholar 

  • 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 65:14–23

    Article  Google Scholar 

  • 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 110:70–78

    Article  Google Scholar 

  • Andrabi M, Vaid A, Razdan VK (2011) Evaluation of different measures to control wilt causing pathogens in chickpea. J Plant Prot Res 51:55–59

    Article  Google Scholar 

  • 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 134:141–149

    Article  PubMed  CAS  Google Scholar 

  • Arabi MIE, Kanacri S, Ayoubi Z, Jawhar M (2013) Mycorrhizal application as a biocontrol agent against common root rot of barley. Res Biotechnol 4:07–12

    Google Scholar 

  • 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 14:121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Auge RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Balaji LP, Ahir RR (2011) Evaluation of plant extracts and biocontrol agents against leaf spot disease of brinjal. Indian Phytopath 64:378–380

    Google Scholar 

  • Barea JM, Azcon-Aguilar C (1982) Production of plant growth-regulating substances by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Appl Environ Microbiol 43:810–813

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barker S, Tagu D (2000) The roles of auxins and cytokinins in mycorrhizal symbioses. J Plant Growth Regul 19:144–154

    CAS  PubMed  Google Scholar 

  • Basu S, Rabara RC, Negi S (2018) AMF: the future prospect for sustainable agriculture. Physiol Mol Plant Pathol 102:36–45

    Article  Google Scholar 

  • Benitez T, Rincon AM, Limon MC, Codon AC (2004) Biocontrol mechanism of Trichoderma strains. Int Microbiol 7:249–260

    CAS  PubMed  Google Scholar 

  • Berg A, Wangun H, Kemami V, Nkengfack AE, Schlegel B (2004) Lignoren, a new sesquiterpenoid metabolite from Trichoderma lignorum HKI 0257. J Basic Microbiol 44:317–319

    Article  CAS  PubMed  Google Scholar 

  • Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1–13

    Article  Google Scholar 

  • 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 22:57–66

    Google Scholar 

  • Bisby GR (1939) Trichoderma viride Pers. ex. Fries, and notes on Hypocrea. Trans Br Mycol Soc 33:149–168

    Article  Google Scholar 

  • BÅ‚aszczyk L, Siwulski M, Sobieralski K, Lisiecka J, JÄ™dryczka M (2014) Trichoderma spp. – application and prospects for use in organic farming and industry. J Plant Prot Res 54:309–317

    Article  Google Scholar 

  • 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 27–44

    Google Scholar 

  • 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 51:1969–1977

    Article  CAS  PubMed  Google Scholar 

  • Bohm H, Albert I, Fan L, Reinhard A, Nurnberger T (2014) Immune receptor complexes at the plant cell surface. Curr Opin Plant Biol 20:47–54

    Article  PubMed  CAS  Google Scholar 

  • 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 280:10–16

    Article  CAS  PubMed  Google Scholar 

  • 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 64:1002–1017

    Article  CAS  PubMed  Google Scholar 

  • Brewer D, Taylor A, Keeping JW, Taha AA, Thaller V (1982) Production of experimental quantities of isocyanide metabolites of Trichoderma hamatum. Can J Microbiol 28:1252–1260

    Article  CAS  PubMed  Google Scholar 

  • Brotman Y, Briff E, Viterbo A, Chet I (2008) Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 147:779–789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:36–41

    Google Scholar 

  • 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:e03766

    Article  PubMed Central  CAS  Google Scholar 

  • 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 8:12–16

    Article  Google Scholar 

  • 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 43:831–834

    Article  CAS  Google Scholar 

  • Castillejo MA, Bani M, Rubiales D (2015) Understanding pea resistance mechanisms in response to Fusarium oxysporum through proteomic analysis. Phytochemistry 115:44–58

    Article  CAS  PubMed  Google Scholar 

  • Cavagnaro TR, Bender SF, Asghari HR, van der Heijden MGA (2015) The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci 20:283–290

    Article  CAS  PubMed  Google Scholar 

  • Chaudhary VB, Sandall EL, Lazarski MV (2018) Urban mycorrhizas: predicting arbuscular mycorrhizal abundance in green roofs. Fungal Ecol:1–8

    Google Scholar 

  • 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 19:1062–1071

    Article  CAS  PubMed  Google Scholar 

  • 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 149:1579–1592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosme M, Ramireddy E, Franken P, Schmülling T, Wurst S (2016) Shoot- and root-borne cytokinin influences arbuscular mycorrhizal symbiosis. Mycorrhiza 26:709–720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 34:467–476

    Article  CAS  Google Scholar 

  • 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 34:4–16

    Article  CAS  Google Scholar 

  • 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 28:97–125

    Article  Google Scholar 

  • 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 87:45–53

    Article  CAS  Google Scholar 

  • 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 581:2367–2374

    Article  PubMed  CAS  Google Scholar 

  • De Hoog GS, Guarro J, Gene J, Figueras MJ (2000) Atlas of Clinical Fungi, vol 1, 2nd edn. Centraalbureau voor Schimmelcultures, Utrecht

    Google Scholar 

  • 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 34:33–38

    Article  Google Scholar 

  • 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 13:414–430

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 17:505–517

    Google Scholar 

  • 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:e1004487

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 112:35–42

    Article  CAS  Google Scholar 

  • 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 13:199–204

    Article  CAS  PubMed  Google Scholar 

  • 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 8:469–480

    Article  CAS  PubMed  Google Scholar 

  • 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 15:174–181

    Article  CAS  Google Scholar 

  • 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 3:1–5

    Article  Google Scholar 

  • 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 9:749–759

    Article  CAS  PubMed  Google Scholar 

  • 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 103:240–250

    Article  Google Scholar 

  • 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 156:79–87

    Article  CAS  Google Scholar 

  • 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 53:12–26

    Article  Google Scholar 

  • 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 31:50–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 12:26–31

    Article  Google Scholar 

  • Escande AR, Laich FS, Pedraza MV (2002) Field testing of honey-bee dispersed Trichoderma spp. to manage sunflower head rot (Sclerotinia sclerotiorum). Plant Pathol 51:346–351

    Article  Google Scholar 

  • 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. http://eur-lex.europa.eu/search.html?qid=1456841738609&text=2009/128&scope=EURLEX&type=quick&lang=en. Accessed Aug 2018

    Google Scholar 

  • 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 5:703–706

    CAS  Google Scholar 

  • Ferrol N, Barea JM, Azcon-Aguilar C (2002) Mechanisms of nutrient transport across interfaces in arbuscular mycorrhizas. Plant Soil 244:231–237

    Article  CAS  Google Scholar 

  • 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 8:1–18

    Article  CAS  Google Scholar 

  • Foo E, Ross JJ, Jones WT, Reid JB (2013) Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 111:769–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fravel D, Olivain C, Alabouvette C (2003) Fusarium oxysporum and its biocontrol. New Phytol 157:493–502

    Article  PubMed  Google Scholar 

  • 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 6:488–498

    Google Scholar 

  • 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 76:20–26

    Article  CAS  Google Scholar 

  • Garcia-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386

    Article  CAS  PubMed  Google Scholar 

  • 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 61:325–337

    Article  CAS  Google Scholar 

  • 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 97:13–20

    Article  Google Scholar 

  • Gianinazzi S, Vosatka M (2004) Inoculum of arbuscular mycorrhizal fungi for production systems: science meets business. Can J Bot 82:1264–1271

    Article  Google Scholar 

  • Giurgiu R, DumitraÈ™ 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 46:260–269

    Article  CAS  Google Scholar 

  • 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 63:3189–3198

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gutkind JS (1998) Cell growth control by G protein-coupled receptors: from signal transduction to signal integration. Oncogene 17:1331–1342

    Article  CAS  PubMed  Google Scholar 

  • 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 23:543–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halder S, Ray MB (2006) Effect of VAM soil containing Glomus fasciculatum on growth of Withania somnifera Dun. Asian J Exp Sci 20:261–268

    CAS  Google Scholar 

  • Hanson LE (2000) Reduction of Verticillium wilt symptoms in cotton following seed treatment with Trichoderma virens. J Cotton Sci 4:224–231

    Google Scholar 

  • 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 28:1961–1974

    Article  CAS  Google Scholar 

  • Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190–194

    Article  CAS  PubMed  Google Scholar 

  • 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, Dordrecht

    Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2(1):43–56

    Article  CAS  PubMed  Google Scholar 

  • 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 60:149–157

    Article  CAS  PubMed  Google Scholar 

  • Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 8:101–110

    Article  CAS  Google Scholar 

  • Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25

    Article  CAS  PubMed  Google Scholar 

  • 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 27:221–230

    Article  CAS  Google Scholar 

  • 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 156:1078–1086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 66:26–36

    Article  CAS  PubMed  Google Scholar 

  • Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10

    Article  CAS  PubMed  Google Scholar 

  • Howell CR (2006) Understanding the mechanisms employed by Trichoderma virens to effect biological control of cotton diseases. Phytopathology 96:178–180

    Article  PubMed  Google Scholar 

  • 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 90:248–252

    Article  CAS  PubMed  Google Scholar 

  • Huang C, Roberts PD, Datnoff LE (2011) Silicon suppresses Fusarium crown and root rot of tomato. J Phytopathol 159:546–554

    Article  CAS  Google Scholar 

  • 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 71:166–173

    Article  CAS  Google Scholar 

  • Jakobsen I (1999) Transport of phosphorus and carbon in arbuscular mycorrhizas. In: Varma A, Hock B (eds) Mycorrhiza. Springer, Berlin

    Google Scholar 

  • 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 3:44–52

    CAS  Google Scholar 

  • 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, IA

    Google Scholar 

  • 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 6:1–13

    Article  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664

    Article  CAS  PubMed  Google Scholar 

  • Kamala T, Indira S (2011) Evaluation of indigenous Trichoderma isolates from Manipur as biocontrol agent against Pythium aphanidermatum on common beans. 3 Biotech 1:217–225

    Article  PubMed  PubMed Central  Google Scholar 

  • Kazan K (2013) Auxin and the integration of environmental signals into plant root development. Ann Bot 112:1655–1665

    Article  PubMed  PubMed Central  Google Scholar 

  • Keymer A, Gutjahr C (2018) Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Curr Opin Plant Biol 44:137–144

    Article  CAS  PubMed  Google Scholar 

  • Khan MH, Meghvansi MK, Panwar V, Gogoi HK, Singh L (2010) Arbuscular mycorrhizal fungi-induced signalling in plant defence against phytopathogens. J Phytol 2:53–69

    Google Scholar 

  • Kieber JJ, Schaller GE (2014) Cytokinins. In: The arabidopsis book. The American Society of Plant Biologists, p e0168

    Google Scholar 

  • 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 119:27–32

    Article  Google Scholar 

  • 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 31:50–60

    Article  PubMed  Google Scholar 

  • 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 52:169–184

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780–790

    Article  CAS  PubMed  Google Scholar 

  • 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 5:1–4

    CAS  Google Scholar 

  • Lambais MR (2006) Unraveling the signaling and signal transduction mechanisms controlling arbuscular mycorrhiza development. Sci Agric 63:405–413

    Article  CAS  Google Scholar 

  • 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 79:174–178

    Article  Google Scholar 

  • 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 12:167–172

    Article  Google Scholar 

  • Li YT, Hwang SG, Huang YM, Huang CH (2018) Effects of Trichoderma asperellum on nutrient uptake and Fusarium wilt of tomato. Crop Prot 110:275–282

    Article  CAS  Google Scholar 

  • 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 67:399–416

    Article  CAS  Google Scholar 

  • 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 99:38–46

    Article  CAS  Google Scholar 

  • 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 50:529–544

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Bucio J, Pelagio-Flores R, Herrera-Estrella A (2015) Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Sci Hortic 196:109–123

    Article  Google Scholar 

  • Lopez-Raez JA, Flors V, Garcia JM, Pozo MJ (2010) AM symbiosis alters phenolic acid content in tomato roots. Plant Signal Behav 5:1–3

    Article  CAS  Google Scholar 

  • 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 169–190

    Chapter  Google Scholar 

  • Ludwig-Muller J, Guther M (2007) Auxins as signals in arbuscular mycorrhiza formation. Plant Signal Behav 2:194–196

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 464:367–373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macho AP, Zipfel C (2014) Plant PRRs and the activation of innate immune signaling. Mol Cell 54:263–273

    Article  CAS  PubMed  Google Scholar 

  • 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 7:595–599

    Google Scholar 

  • 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 89:1843–1850

    Article  CAS  Google Scholar 

  • 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 67:397–408

    Article  CAS  Google Scholar 

  • Mathur N, Vyas A (1995) Influence of VAM on net photosynthesis and transpiration of Ziziphus mauritiana. J Plant Physiol 147:328–330

    Article  CAS  Google Scholar 

  • 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 70:202–206

    Article  Google Scholar 

  • 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 42:185–191

    Article  Google Scholar 

  • Mayer AM (2006) Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67:2318–2331

    Article  CAS  PubMed  Google Scholar 

  • 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 222:709–715

    Article  CAS  PubMed  Google Scholar 

  • 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 32:62–85

    Article  Google Scholar 

  • 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 10:73–78

    Article  Google Scholar 

  • 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 5:1–10

    Article  Google Scholar 

  • 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 162:491–498

    Article  CAS  Google Scholar 

  • 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 20:165–181

    Article  Google Scholar 

  • 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 61:298–305

    Article  CAS  PubMed  Google Scholar 

  • Morkunas I, Gemerek J (2007) The possible involvement of peroxidase in defense of yellow lupin embryo axes against Fusarium oxysporum. J Plant Physiol 164:497–506

    Article  CAS  Google Scholar 

  • 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:e0181630

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mukherjee PK (1997) Trichoderma sp. as a microbial suppressive agent of Sclerotium rolfsii on vegetables. World J Microbiol Biotechnol 13:497–499

    Article  Google Scholar 

  • 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 52:522–529

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 1–9

    Chapter  Google Scholar 

  • Mukherjee PK, Horwitz BA, Herrera-Estrella A, Schmoll M, Kenerley CM (2013b) Trichoderma research in the genome era. Annu Rev Phytopathol 51:105–129

    Article  CAS  PubMed  Google Scholar 

  • 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) 17:625–631

    Article  CAS  Google Scholar 

  • 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 81:664–668

    Article  PubMed  Google Scholar 

  • Nucci M, Anaissie E (2007) Fusarium infections in immunocompromised patients. Clin Microbiol Rev 20:695–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 46:2477–2490

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 63:9–17

    Article  Google Scholar 

  • 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 45:3071–3080

    Google Scholar 

  • 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 25:25–29

    Google Scholar 

  • 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 5:460–464

    Article  Google Scholar 

  • Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  CAS  PubMed  Google Scholar 

  • 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 15:507–514

    Article  CAS  PubMed  Google Scholar 

  • Ponce de Leon I, Montesano M (2013) Activation of defense mechanisms against pathogens in mosses and flowering plants. Int J Mol Sci 14:3178–3200

    Article  CAS  PubMed  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  CAS  PubMed  Google Scholar 

  • 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 205:1431–1436

    Article  CAS  PubMed  Google Scholar 

  • 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 1–7

    Google Scholar 

  • 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 95:212–218

    Article  CAS  PubMed  Google Scholar 

  • 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 133–190

    Chapter  Google Scholar 

  • 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):1461–1468

    Article  CAS  PubMed  Google Scholar 

  • Rahman SFSA, Singh E, Pieterse CMJ, Schenk PM (2018) Emerging microbial biocontrol strategies for plant pathogens. Plant Sci 267:102–111

    Article  CAS  Google Scholar 

  • Raman N, Gnanaguru M, Srinivasan V (2001) Biological control of Fusarium wilt of tomato by VA mycorrhizal fungus Glomus fasciculatum. Bulletin-OILB-SROP 24:33–36

    Google Scholar 

  • Ranf S (2017) Sensing of molecular patterns through cell surface immune receptors. Curr Opin Plant Biol 38:68–77

    Article  CAS  PubMed  Google Scholar 

  • 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 6:4270–4280

    Google Scholar 

  • 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 41:1399–1410

    Article  CAS  Google Scholar 

  • 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 18:74

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rey M, Delgado J, Rincon A, Carmen L, Benitez T, Perez E (2000) Improvement of Trichoderma strains for biocontrol. Rev Iberoam Micol 17:31–36

    Google Scholar 

  • 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 167:869–880

    Article  CAS  PubMed  Google Scholar 

  • Rifai MA (1969) A revision of genus Trichoderma. Commonow Mycol Inst Mycol:116–156

    Google Scholar 

  • 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 2:1–9

    Article  Google Scholar 

  • Roco A, Perez LM (2001) In vitro biocontrol activity of Trichoderma harzianum on Alternaria alternata in the presence of growth regulators. Electron J Biotechnol 4:68–73

    Google Scholar 

  • 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 154:236–244

    Article  CAS  Google Scholar 

  • 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 12:976–984

    Article  CAS  Google Scholar 

  • 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 158:129–138

    Article  CAS  PubMed  Google Scholar 

  • Samuels GJ (1996) Trichoderma: a review of biology and systematic of the genus. Mycol Res 100:923–935

    Article  Google Scholar 

  • 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 94:37–46

    Article  CAS  Google Scholar 

  • 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 103:130–136

    Article  CAS  Google Scholar 

  • 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 137:585–596

    Article  Google Scholar 

  • Sawers RJH, Gutjahr C, Paszkowski U (2007) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13:93–97

    Article  CAS  Google Scholar 

  • 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 16:365–370

    Article  CAS  PubMed  Google Scholar 

  • 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 85:347–351

    Article  CAS  Google Scholar 

  • 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 1837:835–848

    Article  CAS  PubMed  Google Scholar 

  • Schmitz AM, Harrison MJ (2014) Signaling events during initiation of arbuscular mycorrhizal symbiosis. J Integr Plant Biol 56:250–261

    Article  PubMed  Google Scholar 

  • Schmoll M (2008) The information highways of a biotechnological workhorse-signal transduction in Hypocrea jecorina. BMC Genomics 9:430

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 33:115–128

    Article  Google Scholar 

  • Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signaling: reactive oxygen species at the cross-road. Front Plant Sci 7:1–21

    Article  Google Scholar 

  • 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 4:1220–1225

    Google Scholar 

  • Sharma R, Bhat S (2012) Molecular screening of the presence of ech33 from Trichoderma isolate of India. Wudpecker J Agric Res 1:429–432

    Google Scholar 

  • 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 173:345–356

    Article  Google Scholar 

  • 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 10:19898–19907

    CAS  Google Scholar 

  • Sharma V, Salwan R, Sharma PN (2017) The comparative mechanistic aspects of Trichoderma and probiotics: scope for future research. Physiol Mol Plant Pathol 100:84–96

    Article  CAS  Google Scholar 

  • 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 18:287–296

    Article  CAS  PubMed  Google Scholar 

  • Sheng M, Tang M, Zhang F, Huang Y (2011) Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21:423–430

    Article  PubMed  Google Scholar 

  • Sikes BA (2010) When do arbuscular mycorrhizal fungi protect plant roots from pathogens? Plant Signal Behav 5:763–765

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 322

    Google Scholar 

  • 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 43:1495–1503

    Article  Google Scholar 

  • 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 47:10–17

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2002) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, San Diego, CA

    Google Scholar 

  • Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:1–13

    Google Scholar 

  • 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 51:331–342

    Article  CAS  PubMed  Google Scholar 

  • 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 9:1–17

    Article  Google Scholar 

  • 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:e0147625

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 12:1296–1307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tawaraya K, Turjaman M, Ekamawanti HA (2007) Effect of arbuscular mycorrhiza colonization on nitrogen and phosphorus uptake and growth of Aloe vera L. HortSci 42:1737–1739

    Article  Google Scholar 

  • 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 93:745–750

    Google Scholar 

  • 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:https://doi.org/10.5402/2013/601303

    Google Scholar 

  • 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 153:1175–1187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 96:8–20

    Article  Google Scholar 

  • 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 71:5341–5347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 36:2095–2101

    Article  CAS  PubMed  Google Scholar 

  • 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 51:393–400

    Article  Google Scholar 

  • van Loon LC (1997) Induced resistance in plants and the role of pathogenesis-related proteins. Eur J Plant Pathol 103:753–765

    Article  Google Scholar 

  • Van Wees SCM, der Ent SV, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    Article  PubMed  CAS  Google Scholar 

  • 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 1:96–100

    Google Scholar 

  • 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:e988076

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Veresoglou SF, Chen B, Rillig MC (2012) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol Biochem 46:53–62

    Article  CAS  Google Scholar 

  • Verma M, Brar S, Tyagi R, Surampalli R, Valero J (2007) Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J 37:1–20

    Article  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma-plant-pathogen interactions. Soil Biol Biochem 40:1–10

    Article  CAS  Google Scholar 

  • 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 113:58–64

    Article  Google Scholar 

  • Viterbo A, Wiest A, Brotman Y, Chet I, Kenerley C (2007) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746

    Article  CAS  PubMed  Google Scholar 

  • Vos CM, Yang Y, De Coninck B, Cammue BPA (2014) Fungal (-like) biocontrol organisms in tomato disease control. Biol Control 74:65–81

    Article  Google Scholar 

  • Waghmare SJ, Kurundkar BP (2011) Efficacy of local isolates of Trichoderma spp against Fusarium oxysporum sp. carthami causing wilt of safflower. Adv Plant Sci 24:37–38

    Google Scholar 

  • Waghunde RR, Shelake RM, Sabalpara AN (2016) Trichoderma: a significant fungus for agriculture and environment. Afr J Agric Res 11:1952–1965

    Google Scholar 

  • Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Li X, Song F (2012) Protecting cucumber from Fusarium wilt with arbuscular mycorrhizal fungi. Commun Soil Sci Plant Anal 43:2851–2864

    Article  CAS  Google Scholar 

  • Wang W, Shi J, Xie Q, Jiang Y, Yu N, Wang E (2017) Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Mol Plant 10:1147–1158

    Article  CAS  PubMed  Google Scholar 

  • Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291–322

    Article  CAS  PubMed  Google Scholar 

  • 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 274:163–170

    Article  CAS  PubMed  Google Scholar 

  • Weindling R (1932) Trichoderma lignorum as a parasitic of other fungi. Phytopathology 22:837–845

    Google Scholar 

  • 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 108:79–88

    Article  CAS  Google Scholar 

  • Wu QS, Srivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic (Amst) 164:77–87

    Article  CAS  Google Scholar 

  • 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 8:89–101

    Article  CAS  Google Scholar 

  • 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 32:960–967

    Article  CAS  PubMed  Google Scholar 

  • 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 96:97–102

    Article  Google Scholar 

  • Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150

    Article  CAS  PubMed  Google Scholar 

  • Zeilinger S, Gruber S, Bansal R, Mukherjee PK (2016) Secondary metabolism in Trichoderma-chemistry meets genomics. Fungal Biol Rev 30:74–90

    Article  Google Scholar 

  • 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:e0170823

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 23:1–10

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 170:220–224

    Article  PubMed  CAS  Google Scholar 

Download references

Conflicts of Interest

The authors declare no competing and conflict of interest.

Author information

Authors and Affiliations

  1. Department of Botany, Savitribai Phule Pune University, Pune, India

    Khirood Doley & Mahesh Borde

  2. Division of Biochemistry, Department of Chemistry, Savitribai Phule Pune University, Pune, India

    Mohan Kulkarni

Authors
  1. Khirood Doley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mahesh Borde
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohan Kulkarni
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Ajit Varma

  2. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Swati Tripathi

  3. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Ram Prasad

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Doley, K., Borde, M., Kulkarni, M. (2019). AM Fungi and Trichoderma Interaction for Biological Control of Soilborne Plant Pathogen Fusarium oxysporum . In: Varma, A., Tripathi, S., Prasad, R. (eds) Plant Microbe Interface. Springer, Cham. https://doi.org/10.1007/978-3-030-19831-2_4

Download citation

Publish with us

Policies and ethics

Search

Navigation