Endophytic microorganisms for biocontrol of the phytopathogenic fungus Botrytis cinerea

  • Hernando José Bolívar-Anillo
  • Carlos Garrido
  • Isidro G. ColladoEmail author


Botrytis cinerea is the most widely studied necrotrophic phytopathogenic fungus. It causes economic losses that are difficult to calculate due to the large number of hosts. While there are a wide array of fungicides on the market to control this phytopathogen, they are not considered sustainable in terms of the environment and human health. The search for new alternatives to control this phytopathogen has led to the use of endophytic microorganisms as biological control agents. Endophytic bacteria and endophytic fungi have been isolated from different plant species and some have proven effective in inhibiting B. cinerea. Furthermore, a significant number of fungistatic or fungicidal metabolites which could be used as alternative complementary chemical controls have been isolated from these fungi and bacteria. In this review, in addition to the metabolites which have shown fungicide activity against this phytopathogen, the different genera and species of endophytic bacteria and fungi are also considered. These have been isolated from various plant species and have displayed antagonistic activity against B. cinerea.


Antifungal Biological control agents Endophytic fungus and bacteria Grey mould disease 



Biological control agents


Colony forming unit


Half maximal effective concentration


Half maximal inhibitory concentration


Inducing systemic resistance


Minimal inhibitory concentration


Systemic acquired resistance


Volatile organic compounds



  1. Abdel-rahim IR, Abo-elyousr K (2017) Using of endophytic Saccharomycopsis fibuligera and thyme oil for management of gray mold rot of guava fruits. Biol Control 10:124–131CrossRefGoogle Scholar
  2. Aly AH, Debbab A, Kjer J, Proksch P (2010) Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41:1–16CrossRefGoogle Scholar
  3. Andreolli M, Lampis S, Zapparoli G et al (2015) Diversity of bacterial endophytes in 3 and 15 year-old grapevines of Vitis vinifera cv. Corvina and their potential for plant growth promotion and phytopathogen control. Microbiol Res 183:42–52CrossRefGoogle Scholar
  4. Bardin M, Ajouz S, Comby M et al (2015) Is the efficacy of biological control against plant diseases likely to be more durable than that of chemical pesticides? Front Plant Sci 6:1–14CrossRefGoogle Scholar
  5. Barka E, Gognies S, Nowak J et al (2002) Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biol Control 24:135–142CrossRefGoogle Scholar
  6. Boubakri H, Schmitt C (2015) Biocontrol potential of chenodeoxycholic acid (CDCA) and endophytic Bacillus subtilis strains against the most destructive grapevine pathogens. N Z J Crop Hortic Sci 43:261–274CrossRefGoogle Scholar
  7. Bulgarelli D, Schlaeppi K, Spaepen S et al (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838CrossRefGoogle Scholar
  8. Busby P, Ridout M, Newcombe G (2016) Fungal endophytes: modifiers of plant disease. Plant Mol Biol 90:645–655CrossRefGoogle Scholar
  9. Carbú M, González-Rodríguez V, Garrido C et al (2016) New biocontrol strategies for strawberry fungal pathogens. In: Husaini A, Neri D (eds) Strawberry: growth, development and diseases. CABI, BostonGoogle Scholar
  10. Card S, Johnson L, Teasdale S, Caradus J (2016) Deciphering endophyte behaviour: the link between endophyte biology and efficacious biological control agents. FEMS Microbiol Ecol 92:1–20CrossRefGoogle Scholar
  11. Chebotar VK, Malfanova NV, Shcherbakov V et al (2015) Endophytic bacteria in microbial preparations that improve plant development (review). Appl Biochem Microbiol 51:271–277CrossRefGoogle Scholar
  12. Cocq K, Gurr S, Hirsch P, Mauchline T (2017) Exploitation of endophytes for sustainable agricultural intensification. Mol Plant Pathol 8:469–473CrossRefGoogle Scholar
  13. Combés A, Ndoye I, Bance C et al (2012) Chemical communication between the endophytic fungus Paraconiothyrium variabile and the phytopathogen Fusarium oxysporum. PLoS ONE 7:1–11CrossRefGoogle Scholar
  14. Compant S, Duffy B, Nowak J et al (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959CrossRefGoogle Scholar
  15. Contreras M, Loeza PD, Villegas J et al (2016) A glimpse of the endophytic bacterial diversity in roots of blackberry plants (Rubus fruticosus). Genet Mol Res 15:1–10CrossRefGoogle Scholar
  16. Cosoveanu A, Cabrera Y, Hernandez G, Cabrera R (2014) Endophytic fungi from grapevine cultivars in Canary Islands and their activity against phytopatogenic fungi. Int J Agric Crop Sci 7:1497–1503Google Scholar
  17. Dean R, van Kan J, Pretorius ZA et al (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:1–17CrossRefGoogle Scholar
  18. Dutta D, Puzari K, Gogoi R, Dutta P (2014) Endophytes: exploitation as a tool in plant protection. Braz Arch Biol Technol 57:621–629CrossRefGoogle Scholar
  19. Elad Y, Stewart A (2007) Microbial control of Botrytis spp. In: Elad Y, Williamson B, Tudzynski P, Delen N (eds) Botrytis: biology, pathology and control, 1st edn. Springer, New YorkCrossRefGoogle Scholar
  20. Eljounaidi K, Kyu S, Bae H (2016) Bacterial endophytes as potential biocontrol agents of vascular wilt diseases—review and future prospects. Biol Control 103:62–68CrossRefGoogle Scholar
  21. Eun C, Mee J (2016) Endophytic bacteria as biocontrol agents against plant pathogens: current state-of-the-art. Plant Biotechnol Rep 10:353–357CrossRefGoogle Scholar
  22. Farace G, Fernandez O, Jacquens L et al (2015) Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Mol Plant Pathol 16:177–187CrossRefGoogle Scholar
  23. Fouda A, Hassan S, Eid A, Ewais E (2015) Biotechnological applications of fungal endophytes associated with medicinal plant Asclepias sinaica (Bioss.). Ann Agric Sci 60:95–104Google Scholar
  24. Fu J, Zhou Y, Li H et al (2011) Antifungal metabolites from Phomopsis sp. By254, an endophytic fungus in Gossypium hirsutum. Afr J Microbiol Res 5:1231–1236CrossRefGoogle Scholar
  25. Gao Z, Zhang B, Liu H et al (2017) Identification of endophytic Bacillus velezensis ZSY-1 strain and antifungal activity of its volatile compounds against Alternaria solani and Botrytis cinerea. Biol Control 105:27–39CrossRefGoogle Scholar
  26. Glare T, Caradus J, Gelernter W et al (2012) Have biopesticides come of age? Trends Biotechnol 30:250–258CrossRefGoogle Scholar
  27. Haidar R, Fermaud M, Calvo-Garrido C et al (2016) Modes of action for biological control of Botrytis cinerea by antagonistic bacteria. Phytopathol Mediterr 55:13–34Google Scholar
  28. Hardoim P, Overbeek L, Berg G et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320CrossRefGoogle Scholar
  29. He R, Wang G, Liu X et al (2009) Antagonistic bioactivity of an endophytic bacterium isolated from Epimedium brevicornu Maxim. Afr J Biotechnol 8:191–195Google Scholar
  30. Hong CE, Jo SH, Moon JY, Lee J (2015) Isolation of novel leaf-inhabiting endophytic bacteria in Arabidopsis thaliana and their antagonistic effects on phytophathogens. Plant Biotechnol Rep 9:451–458CrossRefGoogle Scholar
  31. Hormazabal E, Piontelli E (2009) Endophytic fungi from Chilean native gymnosperms: antimicrobial activity against human and phytopathogenic fungi. World J Microbiol Biotechnol 25:813–819CrossRefGoogle Scholar
  32. Hung R, Lee S, Bennett J (2015) Fungal volatile organic compounds and their role in ecosystems. Appl Microbiol Biotechnol 99:3395–3405CrossRefGoogle Scholar
  33. Kefi A, Ben Slimene I, Karkouch I et al (2015) Characterization of endophytic Bacillus strains from tomato plants (Lycopersicon esculentum) displaying antifungal activity against Botrytis cinerea Pers. World J Microbiol Biotechnol 31:1967–1976CrossRefGoogle Scholar
  34. Kernaghan G, Mayerhofer M, Griffin A (2017) Fungal endophytes of wild and hybrid Vitis leaves and their potential for vineyard biocontrol. Can J Microbiol 63:583–595CrossRefGoogle Scholar
  35. Kilani-Feki O, Jaoua S (2011) Biological control of Botrytis cinerea using an antagonictic and endophytic Burkholderia cepacia (Cs5) for the vine plantlets protection. Can J Microbiol 57:896–901CrossRefGoogle Scholar
  36. Kusari P, Kusari S, Spiteller M, Kayser O (2013) Endophytic fungi harbored in Cannabis sativa L.: diversity and potential as biocontrol agents against host plant-specific phytopathogens. Fungal Divers 60:137–151CrossRefGoogle Scholar
  37. Kusari P, Kusari S, Spiteller M, Kayser O (2014) Biocontrol potential of endophytes harbored in Radula marginata (liverwort) from the New Zealand ecosystem. Antonie Van Leeuwenhoek 106:771–788CrossRefGoogle Scholar
  38. Lazarovits G, Turnbull A, Johnston-Monje D (2014) Plant health management: biological control of plant pathogens. Encycl Agric Food Syst 4:388–399CrossRefGoogle Scholar
  39. Li X-J, Zhang Q, Zhang A-L, Gao J-M (2012) Metabolites from Aspergillus fumigatus, an endophytic fungus associated with Melia azedarach, and their antifungal, antifeedant, and toxic activities. J Agric Food Chem 60:3424–3431CrossRefGoogle Scholar
  40. Liarzi O, Bar E, Lewinsohn E, Ezra D (2016) Use of the endophytic fungus Daldinia cf. concentrica and its volatiles as bio-control agents. PLoS ONE 11:1–18Google Scholar
  41. Liu B, Huang L, Buchenauer H, Kang Z (2010) Isolation and partial characterization of an antifungal protein from the endophytic Bacillus subtilis strain EDR4. Pestic Biochem Physiol 98:305–311CrossRefGoogle Scholar
  42. Lu XH, Jiao XL, Hao JJ et al (2016) Characterization of resistance to multiple fungicides in Botrytis cinerea populations from Asian ginseng in northeastern China. Eur J Plant Pathol 144:467–476CrossRefGoogle Scholar
  43. Ludwig-Müller J (2015) Plants and endophytes: equal partners in secondary metabolite production? Biotechnol Lett 37:1325–1334CrossRefGoogle Scholar
  44. Mari M, Guizzardi M, Brunelli M, Folchi A (1996) Postharvest biological control of grey mould (Botrytis cinerea Pers.: Fr.) on fresh-market tomatoes with Bacillus amyloliquefaciens. Crop Prot 15:699–705CrossRefGoogle Scholar
  45. Martinez-Hidalgo P, Garcia J, Pozo M (2015) Induced systemic resistance against Botrytis cinerea by Micromonospora strains isolated from root nodules. Front Microbiol 6:1–11CrossRefGoogle Scholar
  46. Miles L, Lopera C, González S et al (2012) Exploring the biocontrol potential of fungal endophytes from an Andean Colombian Paramo ecosystem. Biocontrol 57:697–710CrossRefGoogle Scholar
  47. Miotto-Vilanova L, Jacquard C, Courteaux B et al (2016) Burkholderia phytofirmans PsJN confers grapevine resistance against Botrytis cinerea via a direct antimicrobial effect combined with a better resource mobilization. Front Plant Sci 7:1–15CrossRefGoogle Scholar
  48. Morath S, Hung R, Bennett J (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26:73–83CrossRefGoogle Scholar
  49. Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J 2014:1–11CrossRefGoogle Scholar
  50. Narayan P, Kim W, Woo S et al (2007) Fungal endophytes in roots of Aralia species and their antifungal activity. Plant Pathol J 23:287–294CrossRefGoogle Scholar
  51. Nicot PC, Stewart A, Bardin M, Elad Y (2016) Biological control and biopesticide suppression of Botrytis-incited diseases. In: Fillinger S, Elad Y (eds) Botrytis—the fungus, the pathogen and its management in agricultural systems, 1st edn. Springer, New YorkGoogle Scholar
  52. Noumeur SR, Mancini V, Romanazzi G (2016) Activity of endophytic fungi from Artemisia absinthium on Botrytis cinerea. Acta Hortic 1144:101–104CrossRefGoogle Scholar
  53. O´Brien P (2017) Biological control of plant diseases. Australas Plant Pathol 46:293–304CrossRefGoogle Scholar
  54. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125CrossRefGoogle Scholar
  55. Özer G, Bayraktar H (2014) First report of Botrytis cinerea on Cornelian cherry. Australas Plant Dis Notes 9:2012–2014CrossRefGoogle Scholar
  56. Pan F, Liu Z, Chen Q et al (2016) Endophytic fungus strain 28 isolated from Houttuynia cordata possesses wide-spectrum antifungal activity. Braz J Microbiol 47:480–488CrossRefGoogle Scholar
  57. Park J, Choi G, Lee H et al (2005) Griseofulvin from Xylaria sp. strain F0010, an endophytic fungus of Abies holophylla and its antifungal activity against plant pathogenic fungi. J Microbiol Biotechnol 15:112–117Google Scholar
  58. Park Y, Young J, Jong D et al (2015) Screening and characterization of endophytic fungi of Panax ginseng Meyer for biocontrol activity against ginseng pathogens. Biol Control 91:71–81CrossRefGoogle Scholar
  59. Parnell JJ, Berka R, Young HA et al (2016) From the lab to the farm: an industrial perspective of plant beneficial microorganisms. Front Plant Sci 7:1–12CrossRefGoogle Scholar
  60. Ritika B, Utpal D (2014) An overview of fungal and bacterial biopesticides to control plant pathogens/diseases. Afr J Microbiol Res 8:1749–1762CrossRefGoogle Scholar
  61. Rodríguez A, Acosta A, Rodríguez C (2014) Fungicide resistance of Botrytis cinerea in tomato greenhouses in the Canary Islands and effectiveness of non-chemical treatments against gray mold. World J Microbiol Biotechnol 30:2397–2406CrossRefGoogle Scholar
  62. Rojas-Solís D, Zetter-Salmón E, Contreras-Pérez M et al (2018) Pseudomonas stutzeri E25 and Stenotrophomonas maltophilia CR71 endophytes produce antifungal volatile organic compounds and exhibit additive plant growth-promoting effects. Biocatal Agric Biotechnol 13:46–52CrossRefGoogle Scholar
  63. Romanazzi G, Smilanick J, Feliziani E, Droby S (2016) Integrated management of postharvest gray mold on fruit crops. Postharvest Biol Technol 113:69–76CrossRefGoogle Scholar
  64. Ryan RP, Germaine K, Franks A et al (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9CrossRefGoogle Scholar
  65. Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda M, Glick B (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99CrossRefGoogle Scholar
  66. Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169:18–29CrossRefGoogle Scholar
  67. Schalchli H, Tortella G, Rubilar O et al (2016) Fungal volatiles: an environmentally friendly tool to control pathogenic microorganisms in plants. Crit Rev Biotechnol 36:144–152CrossRefGoogle Scholar
  68. Schena L, Nigro F, Pentimone I et al (2003) Control of postharvest rots of sweet cherries and table grapes with endophytic isolates of Aureobasidium pullulans. Postharvest Biol Technol 30:209–220CrossRefGoogle Scholar
  69. Senthilkumar M, Anandham R, Madhaiyan M et al (2011) Endophytic bacteria: perspectives and applications in agricultural crop production. In: Maheshwari DK (ed) Bacteria in agrobiology: crop ecosystems, 1st edn. Springer, New YorkGoogle Scholar
  70. Soares M, Li H-J, Bergen M et al (2015) Functional role of an endophytic Bacillus amyloliquefaciens in enhancing growth and disease protection of invasive English ivy (Hedera Helix L.). Plant Soil 405:107–123CrossRefGoogle Scholar
  71. Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845–857CrossRefGoogle Scholar
  72. Suprapta DN (2012) Potential of microbial antagonists as biocontrol agents against plant fungal pathogens. J ISSAAS 18:1–8Google Scholar
  73. Suryanarayanan T, Thirunavukkarasu N, Govindarajulu M et al (2009) Fungal endophytes and bioprospecting. Fungal Biol Rev 23:9–19CrossRefGoogle Scholar
  74. Syed Ab Rahman S, Singh E, Pietersen C, Schenck P (2018) Emerging microbial biocontrol strategies for plant pathogens. Plant Sci 267:102–111CrossRefGoogle Scholar
  75. Terhonen E, Sipari N, Asiegbu FO (2016) Inhibition of phytopathogens by fungal root endophytes of Norway spruce. Biol Control 99:53–63CrossRefGoogle Scholar
  76. Toffano L, Batista M, Pascholati S (2017) Potential of fumigation of orange fruits with volatile organic compounds produced by Saccharomyces cerevisiae to control citrus black spot disease at postharvest. Biol Control 108:77–82CrossRefGoogle Scholar
  77. Tomsheck A, Strobel G, Booth E et al (2010) Hypoxylon sp., an endophyte of Persea indica, producing 1,8-cineole and other bioactive volatiles with fuel potential. Microb Ecol 60:903–914CrossRefGoogle Scholar
  78. Trotel-Aziz P, Couderchet M, Biagianti S, Aziz A (2008) Characterization of new bacterial biocontrol agents Acinetobacter, Bacillus, Pantoea and Pseudomonas spp. mediating grapevine resistance against Botrytis cinerea. Environ Exp Bot 64:21–32CrossRefGoogle Scholar
  79. Van J, Shaw M, Grant-Downton R (2014) Botrytis species: relentless necrotrophic thugs or endophytes gone rogue? Mol Plant Pathol 15:957–961Google Scholar
  80. Velivelli S, De Vos P, Kromann P et al (2014) Biological control agents: from field to market, problems, and challenges. Trends Biotechnol 32:493–496CrossRefGoogle Scholar
  81. Wang H, Wen K, Zhao X et al (2009a) The inhibitory activity of endophytic Bacillus sp. strain CHM1 against plant pathogenic fungi and its plant growth-promoting effect. Crop Prot 28:634–639CrossRefGoogle Scholar
  82. Wang S, Hu T, Jiao Y et al (2009b) Isolation and characterization of Bacillus subtilis EB-28, an endophytic bacterium strain displaying biocontrol activity against Botrytis cinerea Pers. Front Agric China 3:247–252CrossRefGoogle Scholar
  83. Williamson B, Tudzynski B, Tudzynnski P, van Kan JA (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8:561–580CrossRefGoogle Scholar
  84. Yang C, Zhang X, Shi G et al (2011) Isolation and identification of endophytic bacterium W4 against tomato Botrytis cinerea and antagonistic activity stability. Afr J Microbiol 5:131–136Google Scholar
  85. Zhang HW, Song YC, Tan RX (2006) Biology and chemistry of endophytes. Nat Prod Rep 23:753–771CrossRefGoogle Scholar
  86. Zhang C, Zheng B, Lao J et al (2008) Clavatol and patulin formation as the antagonistic principle of Aspergillus clavatonanicus, an endophytic fungus of Taxus mairei. Appl Microbiol Biotechnol 78:833–840CrossRefGoogle Scholar
  87. Zhang Q, Zhang J, Yang L et al (2014) Diversity and biocontrol potential of endophytic fungi in Brassica napus. Biol Control 72:98–108CrossRefGoogle Scholar
  88. Zhang X, Zhou Y, Li Y et al (2017) Screening and characterization of endophytic Bacillus for biocontrol of grapevine downy mildew. Crop Prot 96:173–179CrossRefGoogle Scholar
  89. Zhao JH, Zhang YL, Wang LW et al (2012) Bioactive secondary metabolites from Nigrospora sp. LLGLM003, an endophytic fungus of the medicinal plant Moringa oleifera Lam. World J Microbiol Biotechnol 28:2107–2112CrossRefGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Departamento de Química Orgánica, Facultad de CienciasUniversidad de CádizPuerto RealSpain
  2. 2.Laboratorio de Investigación en Microbiología, Facultad de Ciencias Básicas y BiomédicasUniversidad Simón BolívarBarranquillaColombia
  3. 3.Department of Biomedicine and Biotechnology, Laboratory of Microbiology, Faculty of Marine and Environmental SciencesUniversity of CádizPuerto RealSpain

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