Research in Plant Disease (식물병연구)

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Plant Growth Promotion and Biocontrol Potential of Various Phytopathogenic Fungi Using Gut Microbes of Allomyrina dichotoma Larva

장수풍뎅이 유충의 장내 미생물을 이용한 다양한 식물 균류병의 생물적 방제 및 생장촉진

  • Kim, Joon-Young (Department of Plant Science, Gangneung-Wonju National University) ;
  • Kim, Byung-Sup (Department of Plant Science, Gangneung-Wonju National University)
  • 김준영 (강릉원주대학교 식물생명과학과) ;
  • 김병섭 (강릉원주대학교 식물생명과학과)
  • Received : 2020.08.25
  • Accepted : 2020.10.20
  • Published : 2020.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

This research was executed to select beneficial antagonists from digestive organ of Allomyrina dichotoma larva that can be put on environment friendly control against phytopathogenic fungi. We screened 38 bacterial strains inhibiting mycelial growth against eight plant pathogens through dual culture assay. The 10 strains among 38 bacterial strains were selected as beneficial microbes showing antifungal activity against Botrytis cinerea, Plasmodiophora brassicae, Colletotrichum acutatum and Phytophthora capsici through under greenhouse pot trials. The 10 bacterial strains that shown strongest antifungal activity were classified into 3 genera and 10 species, and identified as the genus Bacillus (DM146, DM152, DH2, and DH16), Paenibacillus (DF30, DH14, and DM142) and Streptomyces (DF137, DM48, and DH92) by morphological characteristics and 16s rRNA gene sequence. The 10 bacterial strains had solubilizing activity of insoluble phosphates, production of IAA (indole-3-acetic acid), β-1,3-glucanase and protease. Among the 10 bacterial strains, DM152 strain was produced significant enhancement of all growth parameters of chili pepper and tomato seedlings under greenhouse condition. Thus, this study demonstrated that gut microbes of Allomyrina dichotoma larva will be useful as a potential biocontrol agent against plant pathogens and biofertilizer.

곤충은 장내에 서식하고 있는 미생물과 상호작용을 통해 공생하는 것으로 알려져 있으며, 이러한 공생자는 공진화를 통하여 극한 환경에서도 서식을 가능하게 한다. 이러한 관점에서 토양 속에서 부엽토와 식물 잔재를 먹고 사는 장수풍뎅이 유충의 장내에 존재하는 공생자는 식물병원균을 방제하는 데 유용한 미생물이 존재할 것으로 생각된다. 따라서, 식물병원균에 대해 활성을 갖는 유용 미생물 10종을 장수풍뎅이 유충의 소화기관 전장, 중장, 후장으로부터 분리하였다. 분리된 10종의 유용 미생물은 유묘 검정을 통하여 토마토 잿빛곰팡이병, 배추 뿌리혹병, 고추 탄저병, 고추 역병에 대하여 강력한 항균 활성을 확인하였다. 10종의 항균활성 미생물은 형태적 특성과 16s rRNA gene 분석으로 Bacillus속 4종, Paenibacillus속 3종 및 Streptomyces속 3종으로 동정되었다. 유용 미생물은 인산 가용화, indole-3-acetic acid, siderophore 생성 활성이 우수하며 진균외막가수분해 효소인 β-1,3-glucanase, pretease 활성을 보였다. 10종의 유용 미생물 중, DM152 균주는 토마토와 고추 식물체의 모든 기관에서 생장을 촉진시켰다. 따라서, 장수풍뎅이 유충의 소화기관으로부터 분리된 10종의 장내 미생물은 생물학적 방제제 및 생물비료의 활용 가능성을 나타내었다.

Keywords

References

  1. Andrews, J. H. 1992. Biological control in the phyllosphere. Ann. Rev. Phytopathol. 30: 603-635. https://doi.org/10.1146/annurev.py.30.090192.003131
  2. Chen, J., Abawi, G. S. and Zuckerman, B. M. 2000. Efficacy of Bacillus thuringiensis, Paecilomyces marquandii, and Streptomyces costaricanus with and without organic amendments against Meloidogyne hapla infecting lettuce. J. Nematol. 32: 70-77.
  3. Choi, Y.-H., Lee, K.-Y., Yang, K.-M., Jeong, Y.-M. and Seo, J.-S. 2006. Effect of larva extract of Allomyrina dichotoma on carbon tetrachloride-induced hepatotoxicity in mice. J. Korean Soc. Food Sci. Nutr. 35: 1349-1355. (In Korean) https://doi.org/10.3746/JKFN.2006.35.10.1349
  4. Chung, M. Y., Kwon, E.-Y., Hwang, J.-S., Goo, T.-W. and Yun, E.-Y. 2013. Establishment of food processing methods for larvae of Allomyrina dichotoma, Korean horn beetle. J. Life Sci. 23: 426-431. (In Korean) https://doi.org/10.5352/JLS.2013.23.3.426
  5. De Weger, L. A., van Boxtel, R., van der Burg, B., Gruters, R. A., Geels, F. P., Schippers, B. et al. 1986. Siderophores and outer membrane proteins of antagonistic, plant-growth-stimulating, rootcolonizing Pseudomonas spp. J. Bacteriol. 165: 585-594. https://doi.org/10.1128/jb.165.2.585-594.1986
  6. Dharni, S., Alam, M., Kalani, K., Khaliq, A., Samad, A., Srivastava, S. K. et al. 2012. Production, purification, and characterization of antifungal metabolite from Pseudomonas aeruginosa SD12, a new strain obtained from tannery waste polluted soil. J. Microbiol. Biotechnol. 22: 674-683. https://doi.org/10.4014/jmb.1109.09061
  7. Genta, F. A., Dillon, R. J., Terra, W. R. and Ferreira, C. 2006. Potential role for gut microbiota in cell wall digestion and glucoside de-toxification in Tenebrio molitor larvae. J. Insect. Physiol. 52: 593-601. https://doi.org/10.1016/j.jinsphys.2006.02.007
  8. Hameeda, B., Harini, G., Rupela, O. P., Wani, S. P. and Reddy, G. 2008. Growth promotion of maize by phosphate-solubilizing bacteria isolated from composts and macrofauna. Microbiol. Res. 163: 234-242. https://doi.org/10.1016/j.micres.2006.05.009
  9. Han, J.-H., Park, G.-C., Kim, J.-O. and Kim, K. S. 2015. Biological control of Fusarium stalk rot of maize using Bacillus spp. Res. Plant Dis. 21: 280-289. (In Korean) https://doi.org/10.5423/RPD.2015.21.4.280
  10. Huo, Z., Yang, X., Raza, W., Huang, Q., Xu, Y. and Shen, Q. 2010. Investigation of factors influencing spore germination of Paenibacillus polymyxa ACCC10252 and SQR-21. Appl. Microbiol. Biotechnol. 87: 527-536. https://doi.org/10.1007/s00253-010-2520-8
  11. Kato, K., Kozaki, S. and Sakuranaga, M. 1998. Degradation of lignin compounds by bacteria from termite guts. Biotechnol. Lett. 20: 459-462. https://doi.org/10.1023/A:1005432027603
  12. Kavamura, V. N., Santos, S. N., Silva, J. L., Parma, M. M., Avila, L. A., Visconti, A. et al. 2013. Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol. Res. 168: 183-191. https://doi.org/10.1016/j.micres.2012.12.002
  13. Kumar, R. S., Ayyadurai, N., Pandiaraja, P., Reddy, A. V., Venkateswarlu, Y., Prakash, O. et al. 2005. Characterization of antifungal metabolite produced by a new strain Pseudomonas aeruginosa PUPa3 that exhibits broad-spectrum antifungal activity and biofertilizing traits. J. Appl. Microbiol. 98: 145-154. https://doi.org/10.1111/j.1365-2672.2004.02435.x
  14. Kupferschmied, P., Maurhofer, M. and Keel, C. 2013. Promise for plant pest control: root-associated pseudomonads with insecticidal activities. Front. Plant Sci. 4: 287. https://doi.org/10.3389/fpls.2013.00287
  15. Lacey, L. A. and Georgis, R. 2012. Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. J. Nematol. 44: 218-225.
  16. Lambrecht, M., Okon, Y., Vande Broek, A. and Vanderleyden, J. 2000. Indole-3-acetic acid: a reciprocal signalling molecule in bacteria-plant interactions. Trends Microbiol. 8: 298-300. https://doi.org/10.1016/S0966-842X(00)01732-7
  17. Lee, J. P., Lee, S.-W., Kim, C. S., Son, J. H., Song, J. H., Lee, K. Y. et al. 2006. Evaluation of formulations of Bacillus licheniformis for the biological control of tomato gray mold caused by Botrytis cinerea. Biol. Control 37: 329-337. https://doi.org/10.1016/j.biocontrol.2006.01.001
  18. Lee, H.-W., Ahn, J.-H., Kim, M., Weon, H.-Y., Song, J., Lee, S.-J. et al. 2013. Diversity and antimicrobial activity of actinomycetes from fecal sample of rhinoceros beetle larvae. Korean J. Microbiol. 49: 156-164. (In Korean) https://doi.org/10.7845/kjm.2013.3041
  19. Li, Q., Ning, P., Zheng, L., Huang, J., Li, G. and 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. https://doi.org/10.1016/j.biocontrol.2011.10.014
  20. McSpadden Gardener, B. B. 2004. Ecology of Bacillus and Paenibacillus spp. in agricultural systems. Phytopathology 94: 1252-1258. https://doi.org/10.1094/PHYTO.2004.94.11.1252
  21. Minaxi, L. N., Yadav, R. C. and Saxena, J. 2012. Characterization of multifaceted Bacillus sp. RM-2 for its use as plant growth promoting bioinoculant for crops grown in semi arid deserts. Appl. Soil Ecol. 59: 124-135. https://doi.org/10.1016/j.apsoil.2011.08.001
  22. Moon, C. W., Kim, K. K., Whang, K. S., Seo, M. J., Youn, Y. N. and Yu, Y. M. 2011. Characteristics of Enterobacteria from Harmonia axyridis and effects of Staphylococcus spp. on development of H. axyridis. Korean J. Appl. Entomol. 50: 157-165. (In Korean) https://doi.org/10.5656/KSAE.2011.06.0.30
  23. Nam, H.-S., Yang, H.-J., Oh, B. J., Anderson, A. J. and Kim, Y. C. 2016. Biological control potential of Bacillus amyloliquefaciens KB3 isolated from the feces of Allomyrina dichotoma larvae. Plant Pathol. J. 32: 273-280. https://doi.org/10.5423/PPJ.NT.12.2015.0274
  24. Nicholson, W. L., Munakata, N., Horneck, G., Melosh, H. J. and Setlow, P. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64: 548-572. https://doi.org/10.1128/MMBR.64.3.548-572.2000
  25. Nishiguchi, M. K., Doukakis, P., Egan, M., Kizirian, D., Phillips, A., Prendini, L. et al. 2002. DNA isolation procedures. In: Methods and Tools in Biosciences and Medicine: Techniques in Molecular Systematics and Evolution, eds. by by R. DeSalle, G. Giribet and W. Wheeler, pp. 249-287. Birkhauser Verlag, Basel, Switzerland.
  26. Ntushelo, K., Ledwaba, L. K., Rauwane, M. E., Adebo, O. A. and Njobeh, P. B. 2019. The mode of action of Bacillus species against Fusarium graminearum, tools for investigation, and future prospects. Toxins 11: 606. https://doi.org/10.3390/toxins11100606
  27. Park, D.-S., Oh, H.-W., Bae, K. S., Kim, H., Heo, S.-Y., Kim, N. et al. 2007. Screening of bacteria producing lipase from insect gut: isolation and characterization of a strain, Burkholderia sp. HY-10 producing lipase. Korean J. Appl. Entomol. 46: 131-139. (In Korean) https://doi.org/10.5656/KSAE.2007.46.1.131
  28. Rajagopal, R. 2009. Beneficial interactions between insects and gut bacteria. Indian J. Microbiol. 49: 114-119. https://doi.org/10.1007/s12088-009-0023-z
  29. Rajan, S. S. S., Watkinson, J. H. and Sinclair, A. G. 1996. Phosphate rocks for direct application to soils. Adv. Agron. 57: 77-159. https://doi.org/10.1016/S0065-2113(08)60923-2
  30. Ruffner, B., Péchy-Tarr, M., Ryffel, F., Hoegger, P., Obrist, C., Rindlisbacher, A. et al. 2013. Oral insecticidal activity of plant-associated pseudomonads. Environ. Microbiol. 15: 751-763. https://doi.org/10.1111/j.1462-2920.2012.02884.x
  31. Sanahuja, G., Banakar, R., Twyman, R. M., Capell, T. and Christou, P. 2011. Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol. J. 9: 283-300. https://doi.org/10.1111/j.1467-7652.2011.00595.x
  32. Schwyn, B. and Neilands, J. B. 1997. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160: 47-56. https://doi.org/10.1016/0003-2697(87)90612-9
  33. Shao, Y., Chen, B., Sun, C., Ishida, K., Hertweck, C. and Boland, W. 2017. Symbiont-derived antimicrobials contribute to the control of the lepidopteran gut microbiota. Cell Chem. Biol. 24: 66-75. https://doi.org/10.1016/j.chembiol.2016.11.015
  34. Son, J.-S., Sumayo, M., Hwang, Y.-J., Kim, B.-S. and Ghim, S.-Y. 2014. Screening of plant growth-promoting rhizobacteria as elicitor of systemic resistance against gray leaf spot disease in pepper. Appl. Soil Ecol. 73: 1-8. https://doi.org/10.1016/j.apsoil.2013.07.016
  35. Swain, M. R. and Ray, R. C. 2008. Optimization of cultural conditions and their statistical interpretation for production of indole-3-acetic acid by Bacillus subtilis CM5 using cassava fibrous residue. J. Sci. Ind. Res. 67: 622-628.
  36. Swain, M. R. and Ray, R. C. 2009. Biocontrol and other beneficial activities of Bacillus subtilis isolated from cowdung microflora. Microbiol. Res. 164: 121-130. https://doi.org/10.1016/j.micres.2006.10.009
  37. Torabi, A., Bonjar, G. H. S., Abdolshahi, R., Pournamdari, M., Saadoun, I. and Barka, E. A. 2019. Biological control of Paecilomyces formosus, the causal agent of dieback and canker diseases of pistachio by two strains of Streptomyces misionensis. Biol. Control 137: 104029. https://doi.org/10.1016/j.biocontrol.2019.104029
  38. Vessey, J. K. 2003. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil. 255: 571-586. https://doi.org/10.1023/A:1026037216893
  39. Watanabe, H., Noda, H., Tokuda, G. and Lo, N. 1998. A cellulase gene of termite origin. Nature 394: 330-331. https://doi.org/10.1038/28527
  40. Whipps, J. M. and McQuilken, M. P. 2009. Biological control agents in plant disease control. In: Disease Control in Crops: Biological and Environmentally Friendly Approaches, ed. by D. Walters, pp. 27-61. Wiley-Blackwell, Hoboken, NJ, USA.
  41. Xu, S. J. and Kim, B. S. 2014. Biocontrol of Fusarium crown and root rot and promotion of growth of tomato by Paenibacillus strains isolated from soil. Mycobiology 42: 158-166. https://doi.org/10.5941/myco.2014.42.2.158
  42. Xu, S. J., Park, D. H., Kim, J.-Y. and Kim, B.-S. 2016. Biological control of gray mold and growth promotion of tomato using Bacillus spp. isolated from soil. Trop. Plant Pathol. 41: 169-176. https://doi.org/10.1007/s40858-016-0082-8
  43. Zaidi, S., Usmani, S., Singh, B. R. and Musarrat, J. 2006. Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64: 991-997. https://doi.org/10.1016/j.chemosphere.2005.12.057
  44. Zeriouh, H., Romero, D., Garcia-Gutierrez, L., Cazorla, F. M., de Vicente, A. and Perez-Garcia, A. 2011. The iturin-like lipopeptides are essential components in the biological control arsenal of Bacillus subtilis against bacterial diseases of cucurbits. Mol. Plant-Microbe Interact. 24: 1540-1552. https://doi.org/10.1094/MPMI-06-11-0162