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Overcoming Encouragement of Dragon Fruit Plant (Hylocereus undatus) against Stem Brown Spot Disease Caused by Neoscytalidium dimidiatum Using Bacillus subtilis Combined with Sodium Bicarbonate

  • Ratanaprom, Sanan (Faculty of Science and Technology, Prince of Songkla University, Pattani Campus) ;
  • Nakkanong, Korakot (Agriculture Innovation and Management Division, Faculty of Natural Resources, Prince of Songkla University) ;
  • Nualsri, Charassri (Agriculture Innovation and Management Division, Faculty of Natural Resources, Prince of Songkla University) ;
  • Jiwanit, Palakrit (Faculty of Science and Technology, Prince of Songkla University, Pattani Campus) ;
  • Rongsawat, Thanyakorn (Tropical Fruit and Plantation Crops Research Center, Faculty of Natural Resources, Prince of Songkla University) ;
  • Woraathakorn, Natthakorn (Faculty of Science and Technology, Prince of Songkla University, Pattani Campus)
  • Received : 2021.01.23
  • Accepted : 2021.03.11
  • Published : 2021.06.01

Abstract

The use of the supernatant from a Bacillus subtilis culture mixed with sodium bicarbonate was explored as a means of controlling stem brown spot disease in dragon fruit plants. In in vitro experiments, the B. subtilis supernatant used with sodium bicarbonate showed a strong inhibition effect on the growth of the fungus, Neoscytalidium dimidiatum, the agent causing stem brown spot disease and was notably effective in preventing fungal invasion of dragon fruit plant. This combination not only directly suppressed the growth of N. dimidiatum, but also indirectly affected the development of the disease by eliciting the dragon-fruit plant's defense response. Substantial levels of the pathogenesis-related proteins, chitinase and glucanase, and the phenylpropanoid biosynthetic pathway enzymes, peroxidase and phenyl alanine ammonia-lyase, were triggered. Significant lignin deposition was also detected in treated cladodes of injured dragon fruit plants in in vivo experiments. In summary, B. subtilis supernatant combined with sodium bicarbonate protected dragon fruit plant loss through stem brown spot disease during plant development in the field through pathogenic fungal inhibition and the induction of defense response mechanisms.

Keywords

Acknowledgement

This research was partially funded by the National Research Council of Thailand (NRCT) and Prince of Songkla University (Grant no. SAT6202080S) whose support is gratefully acknowledged. The authors would also like to thank the Publication Clinic, Research and Development Office, Prince of Songkla University, for technical comments and improving the manuscript.

References

  1. Abeles, F. B. and Forrence, L. E. 1970. Temporal and hormonal control of β-1,3-glucanase in Phaseolus vulgaris L. Plant Physiol. 45:395-400. https://doi.org/10.1104/pp.45.4.395
  2. Ali, A., Zahid, N., Manickam, S., Siddiqui, Y., Alderson, P. G. and Maqbool, M. 2014. Induction of lignin and pathogenesis related proteins in dragon fruit plants in response to submicron chitosan dispersions. Crop Prot. 63:83-88. https://doi.org/10.1016/j.cropro.2014.05.009
  3. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  4. Chandrasekaran, M., Paramasivan, M. and Chun, S.-C. 2019. Bacillus subtilis CBR05 induces vitamin B6 biosynthesis in tomato through the de novo pathway in contributing disease resistance against Xanthomonas campestris pv. vesicatoria. Sci. Rep. 9:6495. https://doi.org/10.1038/s41598-019-41888-6
  5. Chuang, M. F., Ni, H. F., Yang, H. R., Shu, S. L., Lai, S. Y. and Jiang, Y. L. 2012. First report of stem canker disease of Pitaya (Hylocereus undatus and H. polyrhizus) caused by Neoscytalidium dimidiatum in Taiwan. Plant Dis. 96:906.
  6. Ezra, D., Liarzi, O., Gat, T., Hershcovich, M. and Dudai, M. 2013. First report of internal black rot caused by Neoscytalidium dimidiatum on Hylocereus undatus (Pitahaya) fruit in Israel. Plant Dis. 97:1513.
  7. Ellis, M. B. 1971. Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew, UK. 608 pp.
  8. Farzaneh, M., Shi, Z.-Q., Ahmadzadeh, M., Hu, L.-B. and Ghassempour, A. 2016. Inhibition of the Aspergillus flavus growth and aflatoxin B1 contamination on pistachio nut by fengycin and surfactin-producing Bacillus subtilis UTBSP1. Plant Pathol. J. 32:209-215. https://doi.org/10.5423/PPJ.OA.11.2015.0250
  9. Fiorin, G. L., Sanchez-Vallet, A., de Toledo Thomazella, D. P., do Prado, P. F. V., do Nascimento, L. C., de Oliveira Figueira, A. V., Thomma, B. P. H. J., Pereira, G. A. G. and Teixeira, P. J. P. L. 2018. Suppression of plant immunity by fungal chitinaselike effectors. Curr. Biol. 28:3023-3030. https://doi.org/10.1016/j.cub.2018.07.055
  10. Gamliel, A., Katan, J. and Cohen, E. 1989. Toxicity of chloronitrobenzenes to Fusarium oxysporum and Rhizoctonia solani as related to their structure. Phytoparasitica 17:101-106. https://doi.org/10.1007/BF02979517
  11. Hazarika, D. J., Goswami, G., Gautom, T., Parveen, A., Das, P., Barooah, M. and Boro, R. C. 2019. Lipopeptide mediated biocontrol activity of endophytic Bacillus subtilis against fungal phytopathogens. BMC Microbiol. 19:71. https://doi.org/10.1186/s12866-019-1440-8
  12. Ippolito, A., Schena, L., Pentimone, I. and Nigro, F. 2005. Control of postharvest rots of sweet cherries by pre- and postharvest applications of Aureobasidium pullulans in combination with calcium chloride or sodium bicarbonate. Postharvest Biol. Technol. 36:245-252. https://doi.org/10.1016/j.postharvbio.2005.02.007
  13. Jiwanit, P., Pitakpornpreecha, T., Pisuchpen, S. and Leelasuphakul, W. 2018. The use of Aloe vera gel coating supplemented with Pichia guilliermondii BCC5389 for enhancement of defense-related gene expression and secondary metabolism in mandarins to prevent postharvest losses from green mold rot. Biol. Control 117:43-51. https://doi.org/10.1016/j.biocontrol.2017.08.023
  14. Lu, Z., Lu, X., Qin, B., Cheng, M., Huang, L., Chen, B. and Liao, Y. 2015. Identification of pathogen of pitaya stem canker disease in Fangchenggang city of Guangxi. J. South. Agric. 46:1606-1612. https://doi.org/10.3969/j:issn.2095-1191.2015.09.1606
  15. Luong, H. T., Kieu, B. T. N., Vu, T. N., Ha, T. T., Van Tong, H., Hua, T. S., Nguyen, N. Q. and Nguyen, T. H. N. 2016. Study on the possibility of using microorganisms as biological agents to control fungal pathogens Neoscytalidium dimidiatum causing disease of brown spots on the dragon fruit. J. Viet. Environ. 8:41-44.
  16. Marin, A., Atares, L. and Chiralt, A. 2017. Improving function of biocontrol agents incorporated in antifungal fruit coatings: a review. Biocontrol Sci. Technol. 27:1220-1241. https://doi.org/10.1080/09583157.2017.1390068
  17. Masratul Hawa, M., Salleh, B. and Latiffah, Z. 2013. Characterization and pathogenicity of Fusarium proliferatum causing stem rot of Hylocereus polyrhizus in Malaysia. Ann. Appl. Biol. 163:269-280. https://doi.org/10.1111/aab.12057
  18. Miller, G. L. 1959. Use of dinitrisalicylic acid reagent for determination of reducing sugars. Anal. Chem. 31:426-428. https://doi.org/10.1021/ac60147a030
  19. Munir, S., Li, Y., He, P., He, P., Ahmed, A., Wu, Y. and He, Y. 2020. Unraveling the metabolite signature of citrus showing defense response towards Candidatus Liberibacter asiaticus after application of endophyte Bacillus subtilis L1-21. Microbiol. Res. 234:126425. https://doi.org/10.1016/j.micres.2020.126425
  20. Sanahuja, G., Lopez, P. and Palmateer, A. J. 2016. First report of Neoscytalidium dimidiatum causing stem and fruit canker of Hylocereus undatus in Florida. Plant Dis. 100:1499-1499. https://doi.org/10.1094/PDIS-11-15-1319-PDN
  21. Sandhu, J. S., Sidhu, M. K. and Yadav, I. S. 2017. Control of fungal diseases in agricultural crops by chitinase and glucanase transgenes. In: Sustainable agriculture reviews, ed. by E. Lichtfouse, pp. 163-212. Springer, Cham, Switzerland.
  22. Spadaro, D. and Droby, S. 2016. Development of biocontrol products for postharvest diseases of fruit: the importance of elucidating the mechanisms of action of yeast antagonists. Trends Food Sci. Technol. 47:39-49. https://doi.org/10.1016/j.tifs.2015.11.003
  23. Tuan, L. N. A., Du, B. D., Ha, L. D. T., Dzung, L. T. K., Phu, D. V. and Hien, N. Q. 2019. Induction of chitinase and brown spot disease tesistance by oligochitosan and nanosilica-oligochitosan in dragon fruit plants. Agric. Res. 8:184-190. https://doi.org/10.1007/s40003-018-0384-9
  24. Ullrich, C., Kluge, B., Palacz, Z. and Vater, J. 1991. Cell-free biosynthesis of surfactin, a cyclic lipopeptide produced by Bacillus subtilis. Biochemistry 30:6503-6508. https://doi.org/10.1021/bi00240a022
  25. Valencia-Botin, A. J., Sandoval-Islas, J. S., Cardenas-Soriano, E., Michailides, T. J. and Rendon-Sanchez, G. 2003. Botryosphaeria dothidea causing stem spots on Hylocereus undatus in Mexico. Plant Pathol. 52:803. https://doi.org/10.1111/j.1365-3059.2003.00912.x
  26. Vallet, C., Chabbert, B., Czaninski, Y. and Monties, B. 1996. Histochemistry of lignin deposition during sclerenchyma differentiation in alfalfa stems. Ann. Bot. 78:625-632. https://doi.org/10.1006/anbo.1996.0170
  27. Waewthongrak, W., Leelasuphakul, W. and McCollum, G. 2014. Cyclic lipopeptides from Bacillus subtilis ABS-S14 elicit defense-related gene expression in citrus fruit. PLoS ONE 9:e109386. https://doi.org/10.1371/journal.pone.0109386
  28. Waewthongrak, W., Pisuchpen, S. and Leelasuphakul, W. 2015. Effect of Bacillus subtilis and chitosan applications on green mold (Penicilium digitatum Sacc.) decay in citrus fruit. Postharvest Biol. Technol. 99:44-49. https://doi.org/10.1016/j.postharvbio.2014.07.016
  29. Wingfield, P. T. 2016. Protein precipitation using ammonium sulfate. Curr. Protoc. Protein Sci. 84:A.3F.1-A.3F.9.
  30. Xu, M., Peng, Y., Qi, Z., Yan, Z., Yang, L., He, M.-D., Li, Q.- X., Liu, C.-L., Ruan, Y.-Z., Wei, S.-S., Xie, J., Xia, Y.-Q. and Tang, H. 2018. Identification of Neoscytalidium dimidiatum causing canker disease of pitaya in Hainan, China. Australas. Plant Pathol. 47:547-553. https://doi.org/10.1007/s13313-018-0588-2
  31. Yi, R. H., Ling Lin, Q., Mo, J. J., Wu, F. F. and Chen, J. 2015. Fruit internal brown rot caused by Neoscytalidium dimidiatum on pitahaya in Guangdong province, China. Australas. Plant Dis. Notes 10:13. https://doi.org/10.1007/s13314-015-0166-1
  32. Youssef, K., Sanzani, S. M., Ligorio, A., Ippolito, A. and Terry, L. A. 2014. Sodium carbonate and bicarbonate treatments induce resistance to postharvest green mould on citrus fruit. Postharvest Biol. Technol. 87:61-69. https://doi.org/10.1016/j.postharvbio.2013.08.006
  33. Zahid, N., Ali, A., Manickam, S., Siddiqui, Y., Alderson, P. G. and Maqbool, M. 2014. Efficacy of curative applications of submicron chitosan dispersions on anthracnose intensity and vegetative growth of dragon fruit plants. Crop Prot. 62:129-134. https://doi.org/10.1016/j.cropro.2014.04.010
  34. Zhang, S., Zheng, Q., Xu, B. and Liu, J. 2019. Identification of the fungal pathogens of postharvest disease on peach fruits and the control mechanisms of Bacillus subtilis JK-14. Toxins 11:322. https://doi.org/10.3390/toxins11060322