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Biological control of tomato gray mold caused by Botrytis cinerea by using Streptomyces spp.

BioControl volume 62, pages 793–803 (2017)Cite this article

Abstract

Streptomyces is a genus known for its ability to protect plants against many pathogens and various strains of this bacteria have been used as biological control agents. In this study, the efficacy of Streptomyces philanthi RM-1-138, S. philanthi RL-1-178, and Streptomyce mycarofaciens SS-2-243 to control various strains of Botrytis cinerea was evaluated both in vitro and in vivo. In vitro studies using confrontation tests on PDA plates indicated that the three strains of Streptomyces spp. inhibited the growth of 41 strains of B. cinerea. Volatile compounds produced by Streptomyces spp. had an influence on the growth of ten strains of B. cinerea while its culture filtrate at low concentration (diluted at 10−3) showed a complete inhibition (100%) of spore germination of B. cinerea strain BC1. A significant protection efficacy of tomato against B. cinerea was observed on both whole plant test (57.4%) and detached leaf test (60.1%) with S. philanti RM-1-138. Moreover, this antagonistic strain had a preventive and a curative effect. These results indicated that S. philanthi RM-1-138 may have the potential to control gray mold caused by B. cinerea on tomato but further work is required to enhance its efficacy and its survival in planta.

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References

  • Ajouz S, Nicot PC, Bardin M (2010) Adaptation to pyrrolnitrin in Botrytis cinerea and cost of resistance. Plant Pathol 59:556–566

    CAS  Article  Google Scholar 

  • Baniasadi F, Bonjar GHS, Baghizadeh A, Karimi Nik A, Jorjandi M, Aghighi S, Farokhi PR (2009) Biological control of Sclerotinia sclerotiorum, causal agent of sunflower head and stem rot disease, by use of soil borne actinomycetes isolates. J Agric Biol Sci 4:146–151

    Article  Google Scholar 

  • Bardin M, Ajouz S, Comby M, Lopez-Ferber M, Graillot B, Siegwart M, Nicot PC (2015) Is the efficacy of biological control against plant diseases likely to be more durable than that of chemical pesticides? Front Plant Sci 6:1–14

    Article  Google Scholar 

  • Boukaew S, Prasertsan P (2014a) Suppression of rice sheath blight disease using heat stable culture filtrate of Streptomyces philanthi RM-1-138. Crop Prot 6:1–10

    Article  Google Scholar 

  • Boukaew S, Prasertsan P (2014b) Factors affecting antifungal activity of Streptomyces philanthi RM-1-138 against Rhizoctonia solani. World J Microbiol Biotechnol 30:323–329

    CAS  Article  PubMed  Google Scholar 

  • Boukaew S, Chuenchit S, Petcharat V (2011) Evaluation of Streptomyces spp. for biological control of Sclerotium root and stem rot and Ralstonia wilt of chili. BioControl 56:365–374

    Article  Google Scholar 

  • Boukaew S, Plubrukarn A, Prasertsan P (2013) Effect of volatile substances from Streptomyces philanthi RM-1-138 on growth of Rhizoctonia solani on rice leaf. BioControl 58:471–482

    CAS  Article  Google Scholar 

  • Chung WH, Ishii H, Nishimura K, Fukaya M, Yano K, Kajitani Y (2006) Fungicide sensitivity and phylogenetic relationship of anthracnose fungi isolated from various fruit crops in Japan. Plant Dis 90:506–512

    CAS  Article  Google Scholar 

  • de Boer W, Gunnewiek PJAK, Lafeber P, Janse JD, Spit BE, Woldendorp JW (1998) Antifungal properties of chitinolytic dune soil bacteria. Soil Biol Biochem 30:193–203

    Article  Google Scholar 

  • Decognet V, Bardin M, Trottin-Caudal Y, Nicot P (2009) Rapid change in the genetic diversity of Botrytis cinerea populations after the introduction of strains in a tomato glasshouse. Phytopathology 99:185–193

    CAS  Article  PubMed  Google Scholar 

  • Elad Y, Pertot I, Cotes Prado AM, Stewart A (2015) Plant hosts of Botrytis spp. In: Fillinger S, Elad Y (eds) Botrytis—the fungus, the pathogen and its management in agricultural systems. Springer, Berlin, pp 413–486

    Google Scholar 

  • Errakhi R, Bouteau F, Lebrihi A, Barakate M (2007) Evidences of biological control capacities of Streptomyces spp. against Sclerotium rolfsii responsible for damping off disease in sugar beet (Beta vulgaris L.). World J Microbiol Biotechnol 23:1503–1509

    CAS  Article  Google Scholar 

  • Fillinger S, Ajouz S, Nicot P, Leroux P, Bardin M (2012) Functional and structural comparison of pyrrolnitrin- and iprodione-induced modifications in the class III histidine-kinase bos1 of Botrytis cinerea. PLoS ONE 7(8):e42520

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Ge BB, Cheng Y, Liu Y, Liu BH, Zhang KC (2015) Biological control of Botrytis cinerea on tomato plants using Streptomyces ahygroscopicus strain CK-15. Lett Appl Microbiol 61:596–602

    CAS  Article  PubMed  Google Scholar 

  • Helbig J (2002) Ability of the antagonistic yeast Cryptococcus albidus to control Botrytis cinerea in strawberry. BioControl 47:85–99

    Article  Google Scholar 

  • Islam MR, Jeong YT, Ryu YJ, Song CH, Lee SY (2009) Identification and optimal culture condition of Streptomyces albidoflavus C247 producing antifungal agents against Rhizoctonia solani AG2-2. Mycobiology 37:114–120

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Jarvis WR (1980) Taxonomy. In: Coley-Smith JR, Verhoeff K, Jarvis WR (eds) The Biology of Botrytis. Academic Press, London, pp 1–17

    Google Scholar 

  • Jiang B, Huang Y, Jia Z, Song S (2016) Streptomyces nobilis C51 suppresses gray mold caused by Botrytis cinerea in tomato. Br Microbiol Res J 16:1–13

    CAS  Article  Google Scholar 

  • Lange L, Sanchez LC (1996) Micro-organisms as a source of biologically active secondary metabolites. In: Copping LG (ed) Crop protection agents from nature: natural products and analogues. R Soc Chem, Cambridge, pp 10–26

    Google Scholar 

  • Lee PJ, Lee SW, Kim CS, Son JH, Song JH, Lee KY, Kim HJ, Jung SJ, Moon JB (2006) Evaluation of formulations of Bacillus licheniformis for the biological control of tomato gray mold caused by Botrytis cinerea. Biol Control 37:329–337

    Article  Google Scholar 

  • Li Q, Ning P, Zheng L, Huang J, Li G, Hsiang T (2010) Fumigant activity of volatiles of Streptomyces globisporus JK-1 against Penicillium italicum on Citrus microcarpa. Postharvest Biol Technol 58:157–165

    CAS  Article  Google Scholar 

  • Li Q, Jiang Y, Ning P, Zheng L, Huang J, Li G, Jiang D, Hsiang T (2011) Suppression of Magnaporthe oryzae by culture filtrates of Streptomyces globisporus JK-1. Biol Control 58:139–148

    CAS  Article  Google Scholar 

  • Li Q, Ning P, Zheng L, Huang J, Li G, Hsiang T (2012) Effects of volatile substances of Streptomyces globisporus JK-1 on control of Botrytis cinerea on tomato fruit. Biol Control 61:113–120

    CAS  Article  Google Scholar 

  • Locke T, Fletcher JT (1988) Incidence of benomyl and iprodione resistance in isolates of Botrytis cinerea in tomato crops in England and Wales in 1986. Plant Pathol 37:381–384

    CAS  Article  Google Scholar 

  • Mahadevan B, Crawford DL (1997) Properties of the chitinase of the antifungal biocontrol agent Streptomyces lydicus WYEC108. Enzym Microbial Technol 20:489–493

    CAS  Article  Google Scholar 

  • Mukherjee G, Sen SK (2006) Purification, characterization, and antifungal activity of chitinase from Streptomyces venezuelae P10. Curr Microbiol 53:265–269

    CAS  Article  PubMed  Google Scholar 

  • Omura S (1992) The expanded horizon for microbial metabolites—a review. Gene 115:141–149

    CAS  Article  PubMed  Google Scholar 

  • Prabavathy VR, Mathivanan N, Murugesan K (2006) Control of blast and sheath blight diseases of rice using antifungal metabolites produced by Streptomyces sp. PM5. Biol Control 39:313–319

    CAS  Article  Google Scholar 

  • Raza W, Yuan J, Ling N, Huang Q, Shen Q (2015) Production of volatile organic compounds by an antagonistic strain Paenibacillus polymyxa WR-2 in the presence of root exudates and organic fertilizer and their antifungal activity against Fusarium oxysporum f. sp. niveum. Biol Control 80:89–95

    CAS  Article  Google Scholar 

  • Sadeghi A, Hessan AR, Askari H, Aghighi S, Bonjar GHS (2006) Biological control potential of two Streptomyces isolates on Rhizoctonia solani, the causal agent of damping-off of sugar beet. I J Biol Sci 9:904–910

    Google Scholar 

  • Vaz Jauri P, Altier N, Kinkel LL (2016) Streptomyces for sustainability. In: Castro-Sowinski S (ed) Microbial models: from environment to industrial sustainability, microorganism for sustainability 1. Springer, Berlin, pp 251–276

    Chapter  Google Scholar 

  • Wu Q, Bai L, Liu W, Li Y, Lu C, Li Y, Fu K, Yu C, Chen J (2013) Construction of a Streptomyces lydicus A01 transformant with a chit42 gene from Trichoderma harzianum P1 and evaluation of its biocontrol activity against Botrytis cinerea. J Microbiol 51:166–173

    CAS  Article  PubMed  Google Scholar 

  • Wu Y, Yuan J, Yaoyao E, Raza W, Shen Q, Huan Q (2015) Effects of volatile organic compounds from Streptomyces albulus NJZJSA2 on growth of two fungal pathogens. J Basic Microbiol 55:1104–1117

    Article  PubMed  Google Scholar 

  • Yourman LF, Jeffers SN (1999) Resistance to Benzimidazole and dicarboximide fungicides in greenhouse isolates of Botrytis cinerea. Plant Dis 83:569–575

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Office of the Higher Education Commission for a scholarship to Mr. Sawai Boukaew under the CHE-PhD Scholarship Program (23/2554) and Thailand Research Fund (RTA5780002).

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Authors and Affiliations

  1. College of Innovation and Management, Songkhla Rajabhat University, Songkhla, 90000, Thailand

    Sawai Boukaew

  2. Department of Industrial Biotechnology, Faculty of Agro-Industry, Prince of Songkla University, Songkhla, 90112, Thailand

    Poonsuk Prasertsan

  3. Pathologie Végétale, INRA, 84140, Montfavet, France

    Sawai Boukaew, Claire Troulet & Marc Bardin

Authors
  1. Sawai Boukaew
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  2. Poonsuk Prasertsan
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  3. Claire Troulet
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  4. Marc Bardin
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Correspondence to Sawai Boukaew or Marc Bardin.

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Handling Editor: Jane Debode.

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Boukaew, S., Prasertsan, P., Troulet, C. et al. Biological control of tomato gray mold caused by Botrytis cinerea by using Streptomyces spp.. BioControl 62, 793–803 (2017). https://doi.org/10.1007/s10526-017-9825-9

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  • DOI: https://doi.org/10.1007/s10526-017-9825-9

Keywords

  • Botrytis cinerea
  • Biological control
  • Durability
  • Sensitivity
  • Streptomyces spp.