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Inhibitory Effects of Pepper Mild Mottle Virus Infection by Supernatants of Five Bacterial Cultures in Capsicum annuum L.

  • Venkata Subba Reddy, Gangireddygari (Virology Unit, Horticulture, and Herbal Crop Environment Division, National Institute of Horticulture and Herbal Science, Rural Development Administration) ;
  • In-Sook, Cho (Virology Unit, Horticulture, and Herbal Crop Environment Division, National Institute of Horticulture and Herbal Science, Rural Development Administration) ;
  • Sena, Choi (Virology Unit, Horticulture, and Herbal Crop Environment Division, National Institute of Horticulture and Herbal Science, Rural Development Administration) ;
  • Ju-Yeon, Yoon (Graduate School on Plant Protection and Quarantine, Jeonbuk National University)
  • Received : 2022.08.12
  • Accepted : 2022.10.31
  • Published : 2022.12.01

Abstract

Pepper mild mottle virus (PMMoV), one of the most prevalent viruses in chili pepper (Capsicum annuum L.) is a non-enveloped, rod-shaped, single-stranded positive-sense RNA virus classified in the genus Tobamovirus. The supernatants of five bacterial cultures (Pseudomonas putida [PP], Bacillus licheniformis [BLI], P. fluorescens [PF], Serratia marcescens [SER], and B. amyloliquifaciens [BA]) were analyzed to find novel antiviral agents to PMMoV in chili pepper. Foliar spraying with supernatants (1:1, v/v) obtained from Luria-Bertani broth cultures of PP, BLI, PF, SER, and BA inhibited PMMoV infection of chili pepper if applied before the PMMoV inoculation. Double-antibody sandwich enzyme-linked immunosorbent assay showed that treatments of five supernatants resulted in 51-66% reductions in PMMoV accumulation in the treated chili pepper. To identify key compounds in supernatants of PP, BLI, PF, SER, and BA, the supernatants were subjected to gas chromatography-mass spectrometry. The 24 different types of compounds were identified from the supernatants of PP, BLI, PF, SER, and BA. The compounds vary from supernatants of one bacterial culture to another which includes simple compounds-alkanes, ketones, alcohols, and an aromatic ring containing compounds. The compounds triggered the inhibitory effect on PMMoV propagation in chili pepper plants. In conclusion, the cultures could be used to further conduct tissue culture and field trial experiments as potential bio-control agents.

Keywords

Acknowledgement

This work was supported by a grant from the Basic Research Program (PJ01431803) of the National Institute of Horticultural and Herbal Science (NIHHS), Rural Development Administration (RDA), Republic of Korea (ROK). The authors are thankful to Dr. Kyeong-Ok Choi, Fruit Research Division, NIHHS, RDA of Korea for the analysis of GC-MS and data discussion.

References

  1. Adam, M., Heuer, H. and Hallmann, J. 2014. Bacterial antagonists of fungal pathogens also control root-knot nematodes by induced systemic resistance of tomato plants. PLoS ONE 9:e90402.
  2. Aguilar, M. I., Guirado, M. L., Melero-Vara, J. M. and Gomez, J. 2010. Efficacy of composting infected plant residues in reducing the viability of Pepper mild mottle virus, Melon necrotic spot virus and its vector, the soil-borne fungus Olpidium bornovanus. Crop. Prot. 29:342-348. https://doi.org/10.1016/j.cropro.2009.12.021
  3. Ait Barka, E., Vatsa, P., Sanchez, L., Gaveau-Vaillant, N., Jacquard, C., Meier-Kolthoff, J. P., Klenk, H.-P., Clement, C., Ouhdouch, Y. and Van Wezel, G. P. 2016. Taxonomy, physiology, and natural products of Actinobacteria. Microbiol. Mol. Biol. Rev. 80:1-43. https://doi.org/10.1128/MMBR.00019-15
  4. Angel, L. P. L., Yusof, M. T., Ismail, I. S., Ping, B. T. Y., Azni, I. N. A. M., Kamarudin, N. H. and Sundram, S. 2016. An in vitro study of the antifungal activity of Trichoderma virens 7b and a profile of its non-polar antifungal components released against Ganoderma boninense. J. Microbiol. 54:732-744. https://doi.org/10.1007/s12275-016-6304-4
  5. Barbieri, E., Gioacchini, A. M., Zambonelli, A., Bertini, L. and Stocchi, V. 2005. Determination of microbial volatile organic compounds from Staphylococcus pasteuri against Tuber borchii using solid-phase microextraction and gas chromatography/ion trap mass spectrometry. Rapid Commun. Mass Spectrom. 19:3411-3415. https://doi.org/10.1002/rcm.2209
  6. Beneduzi, A., Ambrosini, A. and Passaglia, L. M. P. 2012. Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet. Mol. Biol. 35(4 Suppl):1044-1051. https://doi.org/10.1590/S1415-47572012000600020
  7. Brader, G., Compant, S., Mitter, B., Trognitz, F. and Sessitsch, A. 2014. Metabolic potential of endophytic bacteria. Current Opin. Biotechnol. 27:30-37.
  8. Brakhage, A. A. and Schroeckh, V. 2011. Fungal secondary metabolites: strategies to activate silent gene clusters. Fungal Genet. Biol. 48:15-22.
  9. Bruce, A., Stewart, D., Verrall, S. and Wheatley, R. E. 2003. Effect of volatiles from bacteria and yeast on the growth and pigmentation of sapstain fungi. Int. Biodeterior. Biodegrad. 51:101-108. https://doi.org/10.1016/S0964-8305(02)00088-4
  10. Castaldi, S., Cimmino, A., Masi, M. and Evidente, A. 2022. Bacterial lipodepsipeptides and some of their derivatives and cyclic dipeptides as potential agents for biocontrol of pathogenic bacteria and fungi of agrarian plants. J. Agric. Food Chem. 70:4591-4598. https://doi.org/10.1021/acs.jafc.1c08139
  11. Caulier, S., Nannan, C., Gillis, A., Licciardi, F., Bragard, C. and Mahillon, J. 2019. Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Front. Microbiol. 10:302.
  12. Chen, J.-H., Xiang, W., Cao, K.-X., Lu, X., Yao, S.-C., Hung, D., Huang, R.-S. and Li, L.-B. 2020. Characterization of volatile organic compounds emitted from endophytic Burkholderia cenocepacia ETR-B22 by SPME-GC-MS and their inhibitory activity against various plant fungal pathogens. Molecules 25:3765.
  13. Choi, G.-S., Choi, S.-K., Cho, I.-S. and Kwon, S.-J. 2014. Resistance screening to pepper mild mottle virus pathotypes in paprika cultivars. Res. Plant Dis. 20:299-302 (in Korean). https://doi.org/10.5423/RPD.2014.20.4.299
  14. Choudhary, D. K. and Johri, B. N. 2009. Interactions of Bacillus spp. and plants: with special reference to induced systemic resistance (ISR). Microbiol. Res. 164:493-513. https://doi.org/10.1016/j.micres.2008.08.007
  15. Chung, B. N., Kwon, S. J., Choi, G. S., Yoon, J. Y. and Cho, I. S. 2020. Inhibitory effect of cheese whey on cucumber mosaic virus and pepper mottle virus in Capsicum annuum. Res. Plant Dis. 26:103-108. https://doi.org/10.5423/RPD.2020.26.2.103
  16. Ding, Y., Sun, T., Ao, K., Peng, Y., Zhang, Y., Li, X. and Zhang, Y. 2018. Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell 173:1454-1467. https://doi.org/10.1016/j.cell.2018.03.044
  17. Egamberdieva, D., Hashem, A. and Abd-Allah, E. F. 2014. Biological control of fungal disease by rhizobacteria under saline soil conditions. In: Emerging technologies and management of crop stress tolerance, Vol. 2. A sustainable approach, ed. by P. Ahmad and S. Rasool, pp. 161-172. Academic Press, San Diego, CA, USA.
  18. Elsharkawy, M. M., Al-Askar, A. A., Abdelkhalek, A., Behiry, S.I ., Kamran, M. and Ali, M. 2022. Suppression of pepper mild mottle virus (PMMoV) by modified whey proteins. Life 12:1165.
  19. Ferraro, G. B., Suffredini, E., Mancini, P., Veneri, C., Iaconelli, M., Bonadonna, L., Montagna, M. T., De Giglio, O. and La Rosa, G. 2021. Pepper mild mottle virus as indicator for pollution: assessment of prevalence and concentration in different water environments in Italy. Food Environ. Virol. 13:117-125. https://doi.org/10.1007/s12560-020-09458-6
  20. Fu, Z. Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., Mohan, R., Spoel, S. H., Tada, Y., Zheng, N. and Dong, X. 2012. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228-232. https://doi.org/10.1038/nature11162
  21. Gao, H., Li, P., Xu, X., Zeng, Q. and Guan, W. 2018. Research on volatile organic compounds from Bacillus subtilis CF3: biocontrol effects on fruit fungal pathogens and dynamic changes during fermentation. Front. Microbiol. 9:456.
  22. Garbeva, P. and Weisskopf, L. 2020. Airborne medicine: bacterial volatiles and their influence on plant health. New Phytol. 226:32-43. https://doi.org/10.1111/nph.16282
  23. Groenhagen, U., Baumgartner, R., Bailly, A., Gardiner, A., Eberl, L., Schulz, S. and Weisskopf, L. 2013. Production of bioactive volatiles by different Burkholderia ambifaria strains. J. Chem. Ecol. 39:892-906. https://doi.org/10.1007/s10886-013-0315-y
  24. Hung, R., Lee, S. and Bennett, J. W. 2013. Arabidopsis thaliana as a model system for testing the effect of Trichoderma volatile organic compounds. Fungal Ecol. 6:19-26. https://doi.org/10.1016/j.funeco.2012.09.005
  25. Intana, W., Kheawleng, S. and Sunpapao, A. 2021. Trichoderma asperellum T76-14 released volatile organic compounds against postharvest fruit rot in muskmelons (Cucumis melo) caused by Fusarium incarnatum. J. Fungi 7:46.
  26. Jarret, R. L., Gillaspie, A. G., Barkely, N. A. and Pinnow, D. L. 2008. The occurrence and control of pepper mild mottle virus (PMMoV) in the USDA/ARS Capsicum germplasm collection. Seed Technol. 30:26-36.
  27. Kai, M., Haustein, M., Molina, F., Petri, A., Scholz, B. and Piechulla, B. 2009. Bacterial volatiles and their action potential. Appl. Microbiol. Biotechnol. 81:1001-1012. https://doi.org/10.1007/s00253-008-1760-3
  28. Kanchiswamy, C. N., Malnoy, M. and Maffei, M. E. 2015. Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front. Plant Sci. 6:151.
  29. Kang, S. M., Radhakrishnan, R., Lee, K.-E., You, Y.-H., Ko, J.-H., Kim, J.-H. and Lee, I.-J. 2015. Mechanism of plant growth promotion elicited by Bacillus sp. LKE15 in oriental melon. Acta Agric. Scand. Sect. B Soil Plant Sci. 65:637-647.
  30. Kim, J.-S., Lee, S.-H., Choi, H.-S., Kim, M.-K., Kwak, H.-R., Kim, J.-S., Nam, M., Cho, J.-D., Cho, I.-S. and Choi, G.-S. 2012. 2007-2011 Characteristics of plant virus infections on crop samples submitted from agricultural places. Res. Plant Dis. 18:277-289.
  31. Kim, N.-G., Seo, E.-Y., Han, S.-H., Gong, J.-S., Park, C.-N., Park, H.-S., Domier, L. L., Hammond, J. and Lim, H.-S. 2017. Pseudomonas oleovorans strain KBPF-004 culture supernatants reduced seed transmission of cucumber green mottle mosaic virus and pepper mild mottle virus, and remodeled aggregation of 126 kDa and subcellular localization of movement protein of pepper mild mottle virus. Plant Pathol. J. 33:393-401. https://doi.org/10.5423/PPJ.OA.03.2017.0047
  32. Kohl, J., Kolnaar, R. and Ravensberg, W. J. 2019. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front. Plant Sci. 10:845.
  33. Kong, H. G., Shin, T. S., Kim, T. H. and Ryu, C.-M. 2018. Stereoisomers of the bacterial volatile compound 2,3-butanediol differently elicit systemic defense responses of pepper against multiple viruses in the field. Front. Plant Sci. 9:90.
  34. Lee, Y. Y., Lee, Y., Kim, Y. S., Kim, H. S. and Jeon, Y. 2020. Control of red pepper anthracnose using Bacillus subtilis YGB36, a plant growth promoting rhizobacterium. Res. Plant Dis. 26:8-18 (in Korean). https://doi.org/10.5423/RPD.2020.26.1.8
  35. Liu, P., Cheng, Y., Yang, M., Liu, Y., Chen, K., Long, C.-A. and Deng, X. 2014. Mechanisms of action for 2-phenylethanol isolated from Kloeckera apiculata in control of Penicillium molds of citrus fruits. BMC Microbiol. 14:242.
  36. Liu, W., Mu, W., Zhu, B. and Liu, F. 2008. Antifungal activities and components of VOCs produced by Bacillus subtilis G8. Curr. Res. Bacteriol. 1:28-34. https://doi.org/10.3923/crb.2008.28.34
  37. Meziane, H., Van der Sluis, I., Van Loon, L. C., Hofte, M. and Bakker, P. A. H. M. 2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol. Plant Pathol. 6:177-185. https://doi.org/10.1111/j.1364-3703.2005.00276.x
  38. Naamala, J. and Smith, D. L. 2021. Microbial derived compounds, a step toward enhancing microbial inoculants technology for sustainable agriculture. Front. Microbiol. 12:634807.
  39. Petrov, N. 2014. Effect of pepper mild mottle virus infection on pepper and tomato plants. Sci. Technol. 4:61-64.
  40. Piechulla, B., Lemfack, M. C. and Kai, M. 2017. Effects of discrete bioactive microbial volatiles on plants and fungi. Plant Cell Environ. 40:2042-2067.
  41. Pieterse, C. M. J., Van der Does, D., Zamioudis, C., Leon-Reyes, A. and Van Wees, S. C. M. 2011. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489-521. https://doi.org/10.1146/annurev-cellbio-092910-154055
  42. Raaijmakers, J. M. and Mazzola, M. 2012. Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu. Rev. Phytopathol. 50:403-424. https://doi.org/10.1146/annurev-phyto-081211-172908
  43. Radhakrishnan, R., Kang, S.-M., Baek, I.-Y. and Lee, I.-J. 2014. Characterization of plant growth-promoting traits of Penicillium species against the effects of high soil salinity and root disease. J. Plant Interact. 9:754-762. https://doi.org/10.1080/17429145.2014.930524
  44. Radhakrishnan, R., Shim, K.-B., Lee, B.-W., Hwang, C.-D., Pae, S.-B., Park, C.-H., Kim, S.-U., Lee, C.-K. and Baek, I.-Y. 2013. IAA-producing Penicillium sp. NICS01 triggers plant growth and suppresses Fusarium sp.-induced oxidative stress in sesame (Sesamum indicum L.). J. Microbiol. Biotechnol. 23:856-863. https://doi.org/10.4014/jmb.1209.09045
  45. Rialch, N., Sharma, V., Sharma, A. and Sharma, P. N. 2015. Characterization and complete nucleotide sequencing of pepper mild mottle virus infecting bell pepper in India. Phytoparasitica 43:327-337. https://doi.org/10.1007/s12600-015-0453-6
  46. Roberts, P. D. and Adkins, S. 2001. Pepper mild mottle virus. Publication No. HS-808. University of Florida, IFAS Extension, Gainesville, FL, USA. 2 pp.
  47. Ruangwong, O.-U., Pornsuriya, C., Pitija, K. and Sunpapao, A. 2021. Biocontrol mechanisms of Trichoderma koningiopsis PSU3-2 against postharvest anthracnose of chili pepper. J. Fungi 7:276.
  48. Schreiter, S., Ding, G.-C., Heuer, H., Neumann, G., Sandmann, M., Grosch, R., Kropf, S. and Smalla, K. 2014. Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front. Microbiol. 5:144.
  49. Searchinger, T., Waite, R., Hanson, C., Ranganathan, J., Dumas, P. and Matthews, E. 2019. Creating a sustainable food future: a menu of solutions to feed nearly 10 billion people by 2050. World Resources Institute, Washington, DC, USA. 556 pp.
  50. Sharifi, R. and Ryu, C.-M. 2016. Are bacterial volatile compounds poisonous odors to a fungal pathogen Botrytis cinerea, alarm signals to Arabidopsis seedlings for eliciting induced resistance, or both? Front. Microbiol. 7:196.
  51. Song, G. C. and Ryu, C.-M. 2013. Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int. J. Mol. Sci. 14:9803-9819. https://doi.org/10.3390/ijms14059803
  52. Sponsler, D. B., Grozinger, C. M., Hitaj, C., Rundlof, M., Botias, C., Code, A., Lonsdorf, E. V., Melathopoulos, A. P., Smith, D. J., Suryanarayanan, S., Thogmartin, W. E., Williams, N. M., Zhang, M. and Douglas, M. R. 2019. Pesticides and pollinators: a socioecological synthesis. Sci. Total Environ. 662:1012-1027. https://doi.org/10.1016/j.scitotenv.2019.01.016
  53. Syed-Ab-Rahman, S. F., Carvalhais, L. C., Chua, E. T., Chung, F. Y., Moyle, P. M., Eltanahy, E. G. and Schenk, P. M. 2019. Soil bacterial diffusible and volatile organic compounds inhibit Phytophthora capsici and promote plant growth. Sci. Total Environ. 692:267-280. https://doi.org/10.1016/j.scitotenv.2019.07.061
  54. Tahir, H. A. S., Gu, Q., Wu, H., Niu, Y., Huo, R. and Gao, X. 2017. Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Sci. Rep. 7:40481.
  55. Tan, Q.-W., Fang, P.-H., Ni, J.-C., Gao, F. and Chen, Q.-J. 2017. Metabolites produced by an endophytic Phomopsis sp. and their anti-TMV activity. Molecules 22:2073.
  56. Tan, Q.-W., Gao, F.-L., Wang, F.-R. and Chen, Q.-J. 2015. Anti-TMV activity of malformin A1, a cyclic penta-peptide produced by an endophytic fungus Aspergillus tubingensis FJBJ11. Int. J. Mol. Sci. 16:5750-5761. https://doi.org/10.3390/ijms16035750
  57. Thomas, G., Withall, D. and Birkett, M. 2020. Harnessing microbial volatiles to replace pesticides and fertilizers. Microb. Biotechnol. 13:1366-1376. https://doi.org/10.1111/1751-7915.13645
  58. Tilocca, B., Cao, A. and Migheli, Q. 2020. Scent of a killer: microbial volatilome and its role in the biological control of plant pathogens. Front. Microbiol. 11:41.
  59. Tonelli, M. L., Taurian, T., Ibanez, F., Angelini, J. and Fabra, A. 2010. Selection and in vitro characterization of biocontrol agents with potential to protect peanut plants against fungal pathogens. J. Plant Pathol. 92:73-82.
  60. Tsuda, K. and Somssich, I. E. 2015. Transcriptional networks in plant immunity. New Phytol. 206:932-947. https://doi.org/10.1111/nph.13286
  61. United Nations. 2022. World population prospects 2022: summary of results. URL https://www.un.org [11 April 2022].
  62. Vitti, A., Pellegrini, E., Nali, C., Lovelli, S., Sofo, A., Valerio, M., Scopa, A. and Nuzzaci, M. 2016. Trichoderma harzianum T-22 induces systemic resistance in tomato infected by cucumber mosaic virus. Fron. Plant Sci. 7:1520.
  63. Wei, Z., Gu, Y., Friman, V.-P., Kowalchuk, G. A., Xu, Y., Shen, Q. and Jousset, A. 2019. Initial soil microbiome composition and functioning predetermine future plant health. Sci. Adv. 5:eaaw0759.
  64. Wenke, K., Kopka, J., Schwachtje, J., van Dongen, J. T. and Piechulla, B. 2018. Volatiles of rhizobacteria Serratia and Stenotrophomonas alter growth and metabolite composition of Arabidopsis thaliana. Plant Biol. 21(Suppl 1):109-119.
  65. Wetter, C., Conti, M., Altschuh, D., Tabillion, R. and van Regenmortel, M. H. V. 1984. Pepper mild mottle virus, a tobamovirus infecting pepper cultivars in Sicily. Phytopathology 74:405-410. https://doi.org/10.1094/Phyto-74-405
  66. Yoon, J.-Y., Gangireddygari, V. S. R., Cho, I.-S., Chung, B.-N., Yoon, B.-D. and Choi, S.-K. 2021. Effects of ss-glucan from Aureobasidium pullulans on cucumber mosaic virus infection in chili pepper. Res. Plant Dis. 27:17-23. https://doi.org/10.5423/RPD.2021.27.1.17
  67. Zhang, Z.-Z., Li, Y.-B., Qi, L. and Wan X.-C. 2006. Antifungal activities of major tea leaf volatile constituents toward Colletorichum camelliae Massea. J. Agric. Food Chem. 54:3936-3940.  https://doi.org/10.1021/jf060017m