Research in Plant Disease (식물병연구)

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

DOI QR Code

Effects of β-Glucans from Aureobasidium pullulans on Cucumber Mosaic Virus Infection in Chili Pepper

  • Yoon, Ju-Yeon (Horticultural and Herbal Crop Environment Division, National Institute of Horticultural and Herbal Science, Rural Development Administration) ;
  • Gangireddygari, V.S.R. (Horticultural and Herbal Crop Environment Division, National Institute of Horticultural and Herbal Science, Rural Development Administration) ;
  • Cho, In-Sook (Horticultural and Herbal Crop Environment Division, National Institute of Horticultural and Herbal Science, Rural Development Administration) ;
  • Chung, Bong-Nam (Horticultural and Herbal Crop Environment Division, National Institute of Horticultural and Herbal Science, Rural Development Administration) ;
  • Yoon, Byung-Dae (HD Bio-Corporation, KRIBB-BVC) ;
  • Choi, Seung-Kook (Division of Research Planning and Coordination, Rural Development Administration)
  • Received : 2020.11.10
  • Accepted : 2021.01.05
  • Published : 2021.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Cucumber mosaic virus (CMV), the most prevalent virus in chili pepper (Capsicum annuum L.), negatively affects chili pepper production in South Korea. In this study, foliar spraying with β-glucans obtained from the mycelial walls of the yeast-like fungus Aureobasidium pullulans inhibited CMV infection of chili pepper if applied before virus inoculation. At three concentrations, β-glucans from A. pullulans significantly ameliorated CMV symptoms in treated chili pepper; the effect was greater in plants treated with 0.01% β-glucans than 0.005% or 0.001% β-glucans. Double antibody sandwich enzyme-linked immunosorbent assay showed that these β-glucans treatments resulted in 1.7- to 10-fold reductions in CMV accumulation in the treated chili pepper. The glucans did not act directly on the virus and did not interfere with virus disassembly or replication. Foliar spraying with 0.01% β-glucans from A. pullulans at 24 hr intervals for 3 days significantly increased plant height, the total number of fruit, and the fresh weight of chili pepper fruit. However, the stem diameter of chili pepper treated with β-glucans did not increase significantly. These results indicate that foliar spraying with β-glucans from A. pullulans acts an antiviral agent against CMV infection and stimulates chili pepper growth.

Keywords

References

  1. Albersheim, P. and Valent, B. S. 1978. Host-pathogen interactions in plants: plants, when exposed to oligosaccharides of fungal origin, defend themselves by accumulating antibiotics. J. Cell Biol. 78: 627-643. https://doi.org/10.1083/jcb.78.3.627
  2. Ayers, A. R., Ebel, J., Valent, B. and Albersheim, P. 1976. Host-pathogen interactions: X. Fractionation and biological activity of an elicitor isolated from the mycelial walls of Phytophthora megasperma var. sojae. Plant Physiol. 57: 760-765. https://doi.org/10.1104/pp.57.5.760
  3. Aziz, A., Poinssot, B., Daire, X., Adrian, M., Bezier, A., Lambert, B. et al. 2003. Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Mol. Plant Microbe Interact. 16: 1118-1128. https://doi.org/10.1094/MPMI.2003.16.12.1118
  4. Canto, T., Prior, D. A., Hellwald, K. H., Oparka, K. J. and Palukaitis, P. 1997. Characterization of cucumber mosaic virus. IV. Movement protein and coat protein are both essential for cell-to-cell movement of cucumber mosaic virus. Virology 237: 237-248. https://doi.org/10.1006/viro.1997.8804
  5. Caranta, C. and Palloix, A. 1996. Both common and specific genetic factors are involved in polygenic resistance of pepper to several potyviruses. Theor. Appl. Genet. 92: 15-20. https://doi.org/10.1007/bf00222946
  6. Caranta, C., Pflieger, S., Lefebvre, V., Daubeze, A. M., Thabuis, A. and Palloix, A. 2002. QTLs involved in the restriction of Cucumber mosaic virus (CMV) long-distance movement in pepper. Theor. Appl. Genet. 104: 586-591. https://doi.org/10.1007/s001220100753
  7. Cho, J. D., Kim, J. S., Lee, S. H., Choi, G. S. and Chung, B. N. 2007. Viruses and symptoms on peppers, and their infection types in Korea. Res. Plant Dis. 13: 75-81. (In Korean) https://doi.org/10.5423/RPD.2007.13.2.075
  8. Choi, G. S., Kim, J. H., Lee, D. H., Kim, J. S. and Ryu, K. H. 2005. Occurrence and distribution of viruses infecting pepper in Korea. Plant Pathol. J. 21: 258-261. (In Korean) https://doi.org/10.5423/PPJ.2005.21.3.258
  9. Choi, G.-S., Kwon, S.-J., Choi, S.-K., Cho, I.-S. and Yoon, J.-Y. 2015. Characteristics of cucumber mosaic virus-GTN and resistance evaluation of chili pepper cultivars to two cucumber mosaic virus isolates. Res. Plant Dis. 21: 99-102. (In Korean) https://doi.org/10.5423/RPD.2015.21.2.099
  10. Choi, H. K., Song, G. C., Yi, H.-S. and Ryu, C.-M. 2014. Field evaluation of the bacterial volatile derivative 3-pentanol in priming for induced resistance in pepper. J. Chem. Ecol. 40: 882-892. https://doi.org/10.1007/s10886-014-0488-z
  11. Choi, S., Lee, J.-H., Kang, W.-H., Kim, J., Huy, H. N., Park, S.-W. et al. 2018. Identification of cucumber mosaic resistance 2 (cmr2) that confers resistance to a new cucumber mosaic virus isolate P1 (CMV-P1) in pepper (Capsicum spp.). Front. Plant Sci. 9: 1106. https://doi.org/10.3389/fpls.2018.01106
  12. Doolittle, S. P. 1916. A new infectious mosaic disease of cucumber. Phytopathology 6: 145-147.
  13. Ebel, J., Ayers, A. R. and Albersheim, P. 1976. Host-pathogen interactions: XII. Response of suspension-cultured soybean cells to the elicitor isolated from Phytophthora megasperma var. sojae, a fungal pathogen of soybeans. Plant Physiol. 57: 775-779. https://doi.org/10.1104/pp.57.5.775
  14. Fereres, A. and Perry, K. L. 2019. Movement between plants: Horizontal transmission. In: Cucumber Mosaic Virus, eds. by P. Palukaitis and F. Garcia-Arenal, pp. 173-184. The American Phytopathological Society, St. Paul, MN, USA.
  15. Fesel, P. H. and Zuccaro, A. 2016. β-glucan: crucial component of the fungal cell wall and elusive MAMP in plants. Fugal Genet. Biol. 90: 53-60. https://doi.org/10.1016/j.fgb.2015.12.004
  16. Gilbert, W. W. 1916. Cucumber mosaic disease. Phytopathology 6: 143-144.
  17. Giner, A., Pascual, L., Bourgeois, M., Gyetvai, G., Rios, P., Pico, B. et al. 2017. A mutation in the melon Vacuolar Protein Sorting 41 prevents systemic infection of cucumber mosaic virus. Sci. Rep. 7: 10471. https://doi.org/10.1038/s41598-017-10783-3
  18. Grube, R. C., Zhang, Y., Murphy, J. F., Loaiza-Figueroa, F., Lackney, V. K., Provvidenti, R. et al. 2000. New source of resistance to cucumber mosaic virus in Capsicum frutescens. Plant Dis. 84: 885-891. https://doi.org/10.1094/PDIS.2000.84.8.885
  19. Habili, N. and Francki, R. I. B. 1974. Comparative studies on tomato aspermy and cucumber mosaic viruses. II. Virus stability. Virology 60: 29-36. https://doi.org/10.1016/0042-6822(74)90362-6
  20. Hayes, R. J. and Buck, K. W. 1990. Complete replication of a eukaryotic virus RNA in vitro by a purified RNA-dependent RNA polymerase. Cell 63: 363-368. https://doi.org/10.1016/0092-8674(90)90169-f
  21. Heil, M. and Baldwin, I. T. 2002. Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci. 7: 61-67. https://doi.org/10.1016/S1360-1385(01)02186-0
  22. Jagger, I. C. 1916. Experiments with the cucumber mosaic disease. Phytopathology 6: 148-151.
  23. Kang, W.-H., Hoang, N. H., Yang, H.-B., Kwon, J.-K., Jo, S.-H., Seo, J.-K. et al. 2010. Molecular mapping and characterization of a single dominant gene controlling CMV resistance in peppers (Capsicum annuum L.). Theor. Appl. Genet. 120: 1587-1596. https://doi.org/10.1007/s00122-010-1278-9
  24. Kaplan, I. B., Gal-On, A. and Palukaitis, P. 1997. Characterization of cucumber mosaic virus: III. Localization of sequences in the movement protein controlling systemic infection in cucurbits. Virology 230: 343-349. https://doi.org/10.1006/viro.1997.8468
  25. Kazemi, M. 2013. Foliar application of salicylic acid and calcium on yield, yield component and chemical properties of strawberry. Bull. Environ. Pharmacol. Life Sci. 2: 19-23.
  26. Klarzynski, O., Plesse, B., Joubert, J.-M., Yvin, J.-C., Kopp, M., Kloareg, B. et al. 2000. Linear β-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol. 124: 1027-1038. https://doi.org/10.1104/pp.124.3.1027
  27. Kopp, M., Rouster, J., Fritig, B., Darvill, A. and Albersheim, P. 1989. Host-pathogen interactions. Plant Physiol. 90: 208-216. https://doi.org/10.1104/pp.90.1.208
  28. Kwon S.-J., Cho I.-S., Yoon J.-Y. and Chung, B.-N. 2018. Incidence and occurrence pattern of viruses on peppers growing in fields in Korea. Res. Plant Dis. 24: 66-74. https://doi.org/10.5423/RPD.2018.24.1.66
  29. Lapidot, M., Paran, I., Ben-Joseph, R., Ben-Harush, S., Pilowsky, M., Cohen, S. et al. 1997. Tolerance to cucumber mosaic virus in pepper: development of advanced breeding lines and evaluation of virus level. Plant Dis. 81: 185-188. https://doi.org/10.1094/PDIS.1997.81.2.185
  30. Lee, G. H. and Ryu, C.-M. 2016. Spraying of leaf-colonizing Bacillus amyloliquefaciens protects pepper from cucumber mosaic virus. Plant Dis. 100: 2099-2105. https://doi.org/10.1094/PDIS-03-16-0314-RE
  31. Lee, J. H., Hong, J. S., Ju, H.-J. and Park, D. H. 2015. Occurrence of viral diseases in field-cultivated pepper in Korea from 2006 to 2010. Korean J. Org. Agric. 23: 123-131. (In Korean) https://doi.org/10.11625/KJOA.2015.23.1.123
  32. Lee, M. Y., Lee, J. H., Ahn, H. I., Yoon, J. Y., Her, N. H., Choi, J. K. et al. 2006. Identification and sequence analysis of RNA3 of a resistance-breaking cucumber mosaic virus isolate on Capsicum annuum. Plant Pathol. J. 22: 265-270. https://doi.org/10.5423/PPJ.2006.22.3.265
  33. Menard, R., Alban, S., de Ruffray, P., Jamois, F., Franz, G., Fritig, B. et al. 2004. β-1,3 glucan sulfate, but not β-1,3 glucan, induces the salicylic acid signaling pathway in tobacco and Arabidopsis. Plant Cell 16: 3020-3032. https://doi.org/10.1105/tpc.104.024968
  34. Menard, R., de Ruffray, P., Fritig, B., Yvin, J.-C. and Kauffmann, S. 2005. Defense and resistance-inducing activities in tobacco of the sulfated β-1,3 glucan PS3 and its synergistic activities with the unsulfated molecule. Plant Cell Physiol. 46: 1964-1972. https://doi.org/10.1093/pcp/pci212
  35. Muramatsu, D., Okabe, M., Takaoka, A., Kida, H. and Iwai, A. 2017. Aureobasidium pullulans produced β-glucan is effective to enhance Kurosengoku soybean extract induced thrombospondin-1 expression. Sci. Rep. 7: 2831. https://doi.org/10.1038/s41598-017-03053-9
  36. Ngullie, C. R., Tank, R. V. and Bhanderi, D. R. 2014. Effect of salicylic acid and humic acid on flowering, fruiting, yield and quality of mango (Mangifera indica L.) cv. KESAR. Adv. Res. J. Crop Improv. 5: 136-139. https://doi.org/10.15740/HAS/ARJCI/5.2/136-139
  37. Pasternak, T., Groot, E. P., Kazantsev, F. V., Teale, W., Omelyanchuk, N., Kovrizhnykh, V. et al. 2019. Salicylic acid affects root meristem patterning via auxin distribution in a concentration-dependent manner. Plant Physiol. 180: 1725-1739. https://doi.org/10.1104/pp.19.00130
  38. Peden, K. W. C. and Symons, R. H. 1973. Cucumber mosaic virus contains a functionally divided genome. Virology 53: 487-492. https://doi.org/10.1016/0042-6822(73)90232-8
  39. Reunov, A. V., Lapshina, L. A., Nagorskaya, V. P. and Elyakova, L. A. 1996. Effect of 1,3;1,6-β-D-glucan on infection of detached tobacco leaves with tobacco mosaic virus. J. Phytopathol. 144: 247-249. https://doi.org/10.1111/j.1439-0434.1996.tb01524.x
  40. Scholthof, K.-B. G., Adkins, S., Czosnek, H., Palukaitis, P., Jacquot, E., Hohn, T. et al. 2011. Top 10 plant viruses in molecular plant pathology. Mol. Plant Pathol. 12: 938-954. https://doi.org/10.1111/j.1364-3703.2011.00752.x
  41. Sekine, K.-T., Kawakami, S., Hase, S., Kubota, M., Ichinose, Y., Shah, J. et al. 2008. High level expression of a virus resistance gene, RCY 1, confers extreme resistance to cucumber mosaic virus in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 21: 1398-1407. https://doi.org/10.1094/MPMI-21-11-1398
  42. Seo, Y.-S., Rojas, M. R., Lee, J.-Y., Lee, S.-W., Jeon, J.-S., Ronald, P. et al. 2006. A viral resistance gene from common bean functions across plant families and is up-regulated in a non-virus-specific manner. Proc. Natl. Acad. Sci. U. S. A. 103: 11856-11861. https://doi.org/10.1073/pnas.0604815103
  43. Shaaban, M. M., Abd El-Aal, A. M. K. and Ahmed, F. F. 2011. Insight into the effect of salicylic acid on apple trees growing under sandy saline soil. Res. J. Agric. Biol. Sci. 7: 150-156.
  44. Sharp, J. K., McNeil, M. and Albersheim, P. 1984a. The primary structures of one elicitor-active and seven elicitor-inactive hexa(beta-D-glucopyranosyl)-D-glucitols isolated from the mycelial walls of Phytophthora megasperma f. sp. glycinea. J. Biol. Chem. 259: 11321-11336. https://doi.org/10.1016/S0021-9258(18)90865-3
  45. Sharp, J. K., Valent, B. and Albersheim, P. 1984b. Purification and partial characterization of a beta-glucan fragment that elicits phytoalexin accumulation in soybean. J. Biol. Chem. 259: 11312-11320. https://doi.org/10.1016/S0021-9258(18)90864-1
  46. Song, G. C., Choi, H. K. and Ryu, C.-M. 2013. The folate precursor para-aminobenzoic acid elicits induced resistance against cucumber mosaic virus and Xanthomonas axonopodis. Ann. Bot. 111: 925-934. https://doi.org/10.1093/aob/mct049
  47. Statistics Korea. 2019. Production of chili pepper, sesame and highland potatoes in 2019. URL http://kostat.go.kr/ [cited 10 January 2021].
  48. Suzuki, K., Kuroda, T., Miura, Y. and Murai, J. 2003. Screening and field trials of virus resistant sources in Capsicum spp. Plant Dis. 87: 779-783. https://doi.org/10.1094/PDIS.2003.87.7.779
  49. Takahashi, H., Miller, J., Nozaki, Y., Takeda, M., Shah, J., Hase, S. et al. 2002. RCY 1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J. 32: 655-667. https://doi.org/10.1046/j.1365-313X.2002.01453.x
  50. Yoon, J.-Y., Choi, S.-K., Palukaitis, P. and Gray, S. M. 2011. Agrobacterium-mediated infection of whole plants by yellow dwarf viruses. Virus Res. 160: 428-434. https://doi.org/10.1016/j.virusres.2011.06.026
  51. Yoon, J. Y., Paluakaitis, P. and Choi, S. K. 2019. Host range. In: Cucumber Mosaic Cirus, eds. by P. Palukaitis and F. Garcia-Arenal, pp. 15-18. The American Phytopathological Society, St. Paul, MN, USA.