DOI QR코드

DOI QR Code

Induction of systemic resistance in Panax ginseng against Phytophthora cactorum by native Bacillus amyloliquefaciens HK34

  • Lee, Byung Dae (Department of Genetic Engineering, Sungkyunkwan University) ;
  • Dutta, Swarnalee (Division of Agricultural Microbiology, National Academy of Agricultural Sciences, Rural Development Administration) ;
  • Ryu, Hojin (Department of Biology, Chungbuk National University) ;
  • Yoo, Sung-Je (Division of Agricultural Microbiology, National Academy of Agricultural Sciences, Rural Development Administration) ;
  • Suh, Dong-Sang (Department of Genetic Engineering, Sungkyunkwan University) ;
  • Park, Kyungseok (Division of Agricultural Microbiology, National Academy of Agricultural Sciences, Rural Development Administration)
  • Received : 2014.11.13
  • Accepted : 2014.12.18
  • Published : 2015.07.15

Abstract

Background: Korean ginseng (Panax ginseng Meyer) is a perennial herb prone to various root diseases, with Phytophthora cactorum being considered one of the most dreaded pathogens. P. cactorum causes foliar blight and root rot. Although chemical pesticides are available for disease control, attention has been shifted to viable, eco-friendly, and cost-effective biological means such as plant growth-promoting rhizobacteria (PGPR) for control of diseases. Methods: Native Bacillus amyloliquefaciens strain HK34 was isolated from wild ginseng and assessed as a biological control agent for ginseng. Leaves from plants treated with HK34 were analyzed for induced systemic resistance (ISR) against P. cactorum in square plate assay. Treated plants were verified for differential expression of defense-related marker genes using quantitative reverse transcription polymerase chain reaction. Results: A total of 78 native rhizosphere bacilli from wild P. ginseng were isolated. One of the root-associated bacteria identified as B. amyloliquefaciens strain HK34 effectively induced resistance against P. cactorum when applied as soil drench once (99.1% disease control) and as a priming treatment two times in the early stages (83.9% disease control). A similar result was observed in the leaf samples of plants under field conditions, where the percentage of disease control was 85.6%. Significant upregulation of the genes PgPR10, PgPR5, and PgCAT in the leaves of plants treated with HK34 was observed against P. cactorum compared with untreated controls and only pathogen-treated plants. Conclusion: The results of this study indicate HK34 as a potential biocontrol agent eliciting ISR in ginseng against P. cactorum.

Keywords

References

  1. Baeg IH, So SH. The world ginseng market and the ginseng (Korea). J Ginseng Res 2013;37:1-7. https://doi.org/10.5142/jgr.2013.37.1
  2. Lee OR, Sathiyaraj G, Kim YJ, In JG, Kwon WS, Kim JH, Yang DC. Defense genes induced by pathogens and abiotic stresses in Panax ginseng C. A. Meyer. J Ginseng Res 2011;35:1-11. https://doi.org/10.5142/jgr.2011.35.1.001
  3. Kaneko H, Nakanishi K. Proof of the mysterious efficacy of ginseng: basic and clinical trials: clinical effects of medical ginseng, Korean Red Ginseng: specifically, its anti-stress action for prevention of disease. J Pharmacol Sci 2004;95:158-62. https://doi.org/10.1254/jphs.FMJ04001X5
  4. Shin JY, Lee JM, Shin HS, Park SY, Yang JE, Cho SK, Yi TH. Cancer effect of ginsenoside $F_{2}$ against glioblastoma multiforme in xenograft model in SD rats. J Ginseng Res 2012;36:86-92. https://doi.org/10.5142/jgr.2012.36.1.86
  5. Kim JH. Cardiovascular diseases and Panax ginseng: a review on molecular mechanisms and medical applications. J Ginseng Res 2012;36:16-26. https://doi.org/10.5142/jgr.2012.36.1.16
  6. Yuan HD, Kim JT, Kim SH, Chung SH. Ginseng and diabetes: the evidences from in vitro, animal and human studies. J Ginseng Res 2012;36:27-39. https://doi.org/10.5142/jgr.2012.36.1.27
  7. Kim JY, Kim HJ, Kim HJ. Effect of oral administration of Korean Red Ginseng on Influenza A (H1N1) virus infection. J Ginseng Res 2011;35:104-10. https://doi.org/10.5142/jgr.2011.35.1.104
  8. Ryu H, Park H, Suh DS, Jung GH, Park KS, Lee BD. Biological control of Colletotrichum panacicola on Panax ginseng by Bacillus subtilis HK-CSM-1. J Ginseng Res 2014;38:215-9. https://doi.org/10.1016/j.jgr.2014.05.001
  9. Yu YH, Ohh SH. Research on ginseng diseases in Korea. Kor J Ginseng Sci 1993;17:61-8.
  10. Bobev SG, Baeyen S, Crepel C, Martine M. First report of Phytophthora cactorum on American ginseng (Panax quinquefolius) in Bulgaria. Plant Dis 2003;87: 752.
  11. Ohh SH, Yu YH, Kim KH, Cho DH. Studies on control of soil-borne diseases and insects of ginseng and development of antifungal compound. In: Ginseng cultivation bulletin. Kyonggi, Korea: Korean Ginseng and Tobacco Research Institute; 1992. p. 121-84.
  12. Darmono TW, Owen ML, Parke JL. Isolation and pathogenicity of Phytophthora cactorum from forest and ginseng gardens in Wisconsin. Plant Dis 1991;75: 610-2. https://doi.org/10.1094/PD-75-0610
  13. Song M, Yun HY, Kim YH. Antagonistic Bacillus species as a biological control of ginseng root rot caused by Fusarium cf. Incarnatum. J Ginseng Res 2014;38: 136-45. https://doi.org/10.1016/j.jgr.2013.11.016
  14. Bae YS, Park KS, Kim CH. Bacillus spp. as biocontrol agents of root rot and Phytophthora blight on ginseng. Plant Pathol J 2004;20:63-6. https://doi.org/10.5423/PPJ.2004.20.1.063
  15. Haas D, Defago G. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 2005;3:307-19. https://doi.org/10.1038/nrmicro1129
  16. Persello-Cartieaux F, Nussaume L, Robaglia C. Tales from the underground: molecular plant-rhizobacteria interactions. Plant Cell Environ 2003;26:189-99. https://doi.org/10.1046/j.1365-3040.2003.00956.x
  17. Park S, Kloepper JW. Activation of PR-1 a promoter by rhizobacteria that induce systemic resistance in tobacco against Pseudomonas syringae pv. tabaci. Biol Control 2000;18:2-9. https://doi.org/10.1006/bcon.2000.0815
  18. Conrath U, Beckers G, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman M, Pieterse CMJ, Poinssot B, Pozo MJ, et al. Priming: getting ready for battle. Mol Plant Microbe Interac 2006;19:1062-71. https://doi.org/10.1094/MPMI-19-1062
  19. Kumar A, Prakash A, Johri BN. Bacillus as PGPR in crop ecosystem. In: Maheshwari DK, editor. Bacteria in agrobiology: crop ecosystems. Berlin, Germany: Springer-Verlag; 2011. p. 37-59.
  20. Elizabeth ABE, Jo H. Biocontrol of plant disease: a (Gram-) positive perspective. FEMS Microbiol Lett 1999;171:1-9. https://doi.org/10.1111/j.1574-6968.1999.tb13405.x
  21. Ohh SH, Park CS. Studies on Phytophthora disease of Panax ginseng C. A. Meyer; its causal agent and possible control measures. Korean J Ginseng Sci 1980;4:186-93.
  22. Lee SH, Lee JP, Kim KH, Shin HD. Root rot of Japanese angelica caused by Phytophthora cactorum in nursery and mycological characteristics of the isolates. Korean J Mycol 2005;33:98-102. https://doi.org/10.4489/KJM.2005.33.2.098
  23. Kim BS, Lim YS, Kim JH. Leaf blight of Fatsia japonica caused by Phytophthora cactorum. Plant Pathol J 2005;21:293-6. https://doi.org/10.5423/PPJ.2005.21.3.293
  24. Park JW, Balaraju K, Kim JW, Lee SW, Park KS. Systemic resistance and growth promotion of chili pepper induced by an antibiotic producing Bacillus vallismortis strain BS07. Biol Control 2013;65:246-57. https://doi.org/10.1016/j.biocontrol.2013.02.002
  25. Lee OR, Pulla RK, Kim YJ, Balusamy SRD, Yang DC. Expression and stress tolerance of PR10 genes from Panax ginseng C.A. Meyer. Mol Biol Rep 2012;39: 2365-74. https://doi.org/10.1007/s11033-011-0987-8
  26. Kim YJ, Lee JH, Jung DY, Sathiyaraj G, Shim JS, In JG, Yang DC. Isolation and characterization of pathogenesis-related protein 5 (PgPR5) gene from Panax ginseng. Plant Pathol J 2009;25:400-7. https://doi.org/10.5423/PPJ.2009.25.4.400
  27. Ying YX, Ding WL, Li Y. Characterization of soil bacterial communities in rhizospheric and nonrhizospheric soil. Biochem Genet 2012;50:848-59. https://doi.org/10.1007/s10528-012-9525-1
  28. Cho KM, Hong SY, Lee SM, Kim YH, Kahng GG, Lim YP, Kim H, Yun HD. Endophytic bacterial communities in ginseng and their antifungal activity against pathogens. Microb Ecol 2007;54:341-51. https://doi.org/10.1007/s00248-007-9208-3
  29. Li Y, Ying YX, Ding WL. Dynamics of Panax ginseng rhizospheric soil microbial community and their metabolic function. Evid Based Complement Alternat Med 2014;2014:1-7.
  30. Dutta S, Podile AR. Plant growth promoting rhizobacteria (PGPR): bugs to debug the root zone. Crit Rev Microbiol 2010;36:232-44. https://doi.org/10.3109/10408411003766806
  31. Das SN, Dutta S, Anil K, Neeraja C, Sarma PVSRN, Srinivas V, Podile AR. Plant growth-promoting chitinolytic Paenibacillus elgii responds positively to the tobacco root exudates. J Plant Growth Regul 2010;29:409-18. https://doi.org/10.1007/s00344-010-9152-1
  32. Garbeva P, van Veen JA, van Elsas JD. Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 2004;42:243-70. https://doi.org/10.1146/annurev.phyto.42.012604.135455
  33. Weiland G, Neumann R, Backhaus H. Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. Appl Environ Microbiol 2001;67:5849-54. https://doi.org/10.1128/AEM.67.12.5849-5854.2001
  34. Lee BD, Park H. Relationship between plant protection rate and coefficient of variation of microbial products for ginseng cultivation. J Ginseng Res 2009;33: 127-31. https://doi.org/10.5142/JGR.2009.33.2.127
  35. Hill SN, Hausbeck MK. Virulence and fungicide sensitivity of Phytophthora cactorum isolated from American ginseng gardens in Wisconsin and Michigan. Plant Dis 2008;92:1183-9. https://doi.org/10.1094/PDIS-92-8-1183
  36. El-Kereamy A, Jayasankar S, Taheri A, Errampalli D, Paliyath G. Expression analysis of a plum pathogenesis-related 10 (PR10) protein during brown rot infection. Plant Cell Rep 2009;28:95-102. https://doi.org/10.1007/s00299-008-0612-z
  37. Kim ST, Yu S, Kang YH, Kim SG, Kim JY, Kim SH, Kang KY. The rice pathogen related protein 10 (JIOsPR10) is induced by abiotic and biotic stresses and exhibits ribonuclease activity. Plant Cell Rep 2008;27:593-603. https://doi.org/10.1007/s00299-007-0485-6
  38. Liu JJ, Ekramoddoullah AKM. The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 2006;68:3-13. https://doi.org/10.1016/j.pmpp.2006.06.004
  39. Pulla RK, Lee OR, In JG, Kim YJ, Senthil K, Yang DC. Expression and functional characterization of pathogenesis related protein family 10 gene, PgPR10-2, from Panax ginseng C.A. Meyer. Physiol Mol Plant Pathol 2010;74:323-9. https://doi.org/10.1016/j.pmpp.2010.05.001
  40. Xie YR, Chen ZY, Brown RL, Bhatnagar D. Expression and functional characterization of two pathogenesis-related protein 10 genes from Zea mays. J Plant Physiol 2010;167:121-30. https://doi.org/10.1016/j.jplph.2009.07.004
  41. Park CJ, Kim KJ, Shin R, Park JM, Shin YC, Paek KH. Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant J 2004;37:186-98. https://doi.org/10.1046/j.1365-313X.2003.01951.x
  42. Vigers AJ, Roberts WK, Selitrennikoff CP. A new family of plant antifungal proteins. Mol Plant Microbe Interact 1991;4:315-23. https://doi.org/10.1094/MPMI-4-315
  43. Purev M, Kim YJ, Kim MK, Pulla RK, Yang DC. Isolation of a novel catalase (Cat1) gene from Panax ginseng and analysis of the response of this gene to various stresses. Physiol Biochem 2010;48:451-60.
  44. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 2010;33:453-67. https://doi.org/10.1111/j.1365-3040.2009.02041.x
  45. Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004;55:373-99. https://doi.org/10.1146/annurev.arplant.55.031903.141701
  46. Sathiyaraj G, Lee OR, Parvin S, Khorolragchaa A, Kim YJ, Yang DC. Transcript profiling of antioxidant genes during biotic and abiotic stresses in Panax ginseng C.A. Meyer. Mol Biol Rep 2011;38:2761-9. https://doi.org/10.1007/s11033-010-0421-7

Cited by

  1. BTH 처리한 배배양 인삼에서 주요 진균병 저항성 증진 효과 vol.43, pp.1, 2015, https://doi.org/10.5010/jpb.2016.43.1.99
  2. Bacillus species as versatile weapons for plant pathogens: a review vol.31, pp.3, 2015, https://doi.org/10.1080/13102818.2017.1286950
  3. Belowground Microbiota and the Health of Tree Crops vol.9, pp.None, 2015, https://doi.org/10.3389/fmicb.2018.01006
  4. Transcription profiling and identification of infection-related genes in Phytophthora cactorum vol.293, pp.2, 2018, https://doi.org/10.1007/s00438-017-1400-7
  5. Efficacy of Bacillus subtilis native strains for biocontrol of Phytophthora crown and root rot of pistachio in Iran vol.43, pp.4, 2015, https://doi.org/10.1007/s40858-018-0226-0
  6. Potential of combined biological control agents to cope with Phytophthora parasitica, a major pathogen of Choisya ternata vol.152, pp.4, 2018, https://doi.org/10.1007/s10658-018-1495-7
  7. The impact of microbes in the orchestration of plants’ resistance to biotic stress: a disease management approach vol.103, pp.1, 2019, https://doi.org/10.1007/s00253-018-9433-3
  8. Biofertilizers regulate the soil microbial community and enhance Panax ginseng yields vol.14, pp.None, 2015, https://doi.org/10.1186/s13020-019-0241-1
  9. Potential of Pseudomonas putida, Bacillus subtilis, and their mixture on the management of Meloidogyne incognita, Pectobacterium betavasculorum, and Rhizoctonia solani disease complex of beetroot (Bet vol.29, pp.1, 2015, https://doi.org/10.1186/s41938-019-0174-0
  10. Pseudomonas fluorescens MZ05 Enhances Resistance against Setosphaeria turcica by Mediating Benzoxazinoid Metabolism in the Maize Inbred Line Anke35 vol.10, pp.2, 2015, https://doi.org/10.3390/agriculture10020032
  11. Cover Crop Diversity as a Tool to Mitigate Vine Decline and Reduce Pathogens in Vineyard Soils vol.12, pp.4, 2015, https://doi.org/10.3390/d12040128
  12. Mecanismos de acción de Bacillus spp. (Bacillaceae) contra microorganismos fitopatógenos durante su interacción con plantas vol.25, pp.1, 2015, https://doi.org/10.15446/abc.v25n1.75045
  13. Current scenario and future prospects of plant growth-promoting rhizobacteria: an economic valuable resource for the agriculture revival under stressful conditions vol.43, pp.20, 2015, https://doi.org/10.1080/01904167.2020.1799004
  14. A Novel Biocontrol Strain Bacillus amyloliquefaciens FS6 for Excellent Control of Gray Mold and Seedling Diseases of Ginseng vol.105, pp.7, 2015, https://doi.org/10.1094/pdis-07-20-1593-re