Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

Pathogenesis strategies and regulation of ginsenosides by two species of Ilyonectria in Panax ginseng: power of speciation

  • Farh, Mohamed El-Agamy (Graduate School of Biotechnology, College of Life Science, Kyung Hee University) ;
  • Kim, Yu-Jin (Department of Oriental Medicinal Biotechnology, College of Life Sciences, Kyung Hee University) ;
  • Abbai, Ragavendran (Graduate School of Biotechnology, College of Life Science, Kyung Hee University) ;
  • Singh, Priyanka (Department of Oriental Medicinal Biotechnology, College of Life Sciences, Kyung Hee University) ;
  • Jung, Ki-Hong (Graduate School of Biotechnology, College of Life Science, Kyung Hee University) ;
  • Kim, Yeon-Ju (Graduate School of Biotechnology, College of Life Science, Kyung Hee University) ;
  • Yang, Deok-Chun (Graduate School of Biotechnology, College of Life Science, Kyung Hee University)
  • Received : 2017.12.26
  • Accepted : 2019.02.13
  • Published : 2020.03.15
Download PDF
⟨ Previous Next ⟩

Abstract

Background: The valuable medicinal plant Panax ginseng has high pharmaceutical efficacy because it produces ginsenosides. However, its yields decline because of a root-rot disease caused by Ilyonectria mors-panacis. Because species within Ilyonectria showed variable aggressiveness by altering ginsenoside concentrations in inoculated plants, we investigated how such infections might regulate the biosynthesis of ginsenosides and their related signaling molecules. Methods: Two-year-old ginseng seedlings were treated with I. mors-panacis and I. robusta. Roots from infected and pathogen-free plants were harvested at 4 and 16 days after inoculation. We then examined levels or/and expression of genes of ginsenosides, salicylic acid (SA), jasmonic acid (JA), and reactive oxygen species (ROS). We also checked the susceptibility of those pathogens to ROS. Results: Ginsenoside biosynthesis was significantly suppressed and increased in response to infection by I. mors-panacis and I. robusta, respectively. Regulation of JA was significantly higher in I. robusta-infected roots, while levels of SA and ROS were significantly higher in I. mors-panacis-infected roots. Catalase activity was significantly higher in I. robusta-infected roots followed in order by mock roots and those infected by I. mors-panacis. Moreover, I. mors-panacis was resistant to ROS compared with I. robusta. Conclusion: Infection by the weakly aggressive I. robusta led to the upregulation of ginsenoside production and biosynthesis, probably because only a low level of ROS was induced. In contrast, the more aggressive I. mors-panacis suppressed ginsenoside biosynthesis, probably because of higher ROS levels and subsequent induction of programmed cell death pathways. Furthermore, I. mors-panacis may have increased its virulence by resisting the cytotoxicity of ROS.

Keywords

References

  1. Byford W, Gambogi P. Phoma and other fungi on beet seed. Trans Br Mycol Soc 1985;84(1):21-8. https://doi.org/10.1016/s0007-1536(85)80215-1
  2. Dillard H, Hunter J. Association of common ragweed with Sclerotinia rot of cabbage in New York State. Plant Dis 1986;70(1):26-8. https://doi.org/10.1094/PD-70-26
  3. Farh ME-A, Kim Y-J, Kim Y-J, Yang D-C. Cylindrocarpon destructans/Ilyonectria radicicola-species complex: causative agent of ginseng root-rot disease and rusty symptoms. J Ginseng Res 2019;42(1):9-15. https://doi.org/10.1016/j.jgr.2017.01.004
  4. Gerlagh M, Blok W. Fusarium oxysporum f. sp. cucurbitacearum n.f. embracing all formae speciales of F. oxysporum attacking cucurbitaceous crops. Eur J Plant Pathol 1988;94(1):17-31.
  5. Johnston S, Springer J, Lewis G. Fusarium moniliforme as a cause of stem and crown rot of asparagus and its association with asparagus decline. Phytopathology 1979;69(7):778-80. https://doi.org/10.1094/Phyto-69-778
  6. Ohh S, Park C. Studies on Phytophthora disease of Panax ginseng CA Meyer: its causal agent and possible control measure. Korean J Ginseng Sci 1980.
  7. Papavizas GC. Aphanomyces species and their root diseases in pea and sugarbeet: a review: agricultural Research Service. US Department of Agriculture; 1974.
  8. Trapero-Casas A, Jimenez-Diaz RM. Fungal wilt and root rot diseases of chickpea in southern Spain. Phytopathology 1985;75(1):146-1151.
  9. Das K, Roychoudhury A. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Redox Homeostasis Managers in Plants under Environmental Stresses. 2016. p. 53.
  10. Desikan R, Soheila A-H, Hancock JT, Neill SJ. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 2001;127(1):159-72. https://doi.org/10.1104/pp.127.1.159
  11. Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:2012.
  12. Yan J, Tsuichihara N, Etoh T, Iwai S. Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening. Plant Cell Environ 2007;30(10):1320-5. https://doi.org/10.1111/j.1365-3040.2007.01711.x
  13. Maheshwari R, Dubey R. Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul 2009;59(1):37-49. https://doi.org/10.1007/s10725-009-9386-8
  14. Meriga B, Reddy BK, Rao KR, Reddy LA, Kishor PK. Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol 2004;161(1):63-8. https://doi.org/10.1078/0176-1617-01156
  15. Mishra S, Jha A, Dubey R. Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma 2011;248(3):565-77. https://doi.org/10.1007/s00709-010-0210-0
  16. Shah K, Kumar RG, Verma S, Dubey R. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 2001;161(6):1135-44. https://doi.org/10.1016/S0168-9452(01)00517-9
  17. Sharma P, Dubey RS. Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul 2005;46(3):209-21. https://doi.org/10.1007/s10725-005-0002-2
  18. Verma S, Dubey R. Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 2003;164(4):645-55. https://doi.org/10.1016/S0168-9452(03)00022-0
  19. Desmond OJ, Manners JM, Stephens AE, Maclean DJ, Schenk PM, Gardiner DM, Munn AL, Kazan K. The Fusarium mycotoxin deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defence responses in wheat. Mol Plant Pathol 2008;9(4):435-45. https://doi.org/10.1111/j.1364-3703.2008.00475.x
  20. Rossi FR, Garriz A, Marina M, Romero FM, Gonzalez ME, Collado IG, Pieckenstain FL. The sesquiterpene botrydial produced by Botrytis cinerea induces the hypersensitive response on plant tissues and its action is modulated by salicylic acid and jasmonic acid signaling. Mol Plant-Microbe In 2011;24(8):888-96. https://doi.org/10.1094/MPMI-10-10-0248
  21. Shlezinger N, Minz A, Gur Y, Hatam I, Dagdas YF, Talbot NJ, Sharon A. Antiapoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection. PLoS Pathog 2011;7(8):e1002185. https://doi.org/10.1371/journal.ppat.1002185
  22. Chen Q, Zhang M, Shen S. Effect of salt on malondialdehyde and antioxidant enzymes in seedling roots of Jerusalem artichoke (Helianthus tuberosus L.). Acta Physiol Plant 2011;33(2):273-8. https://doi.org/10.1007/s11738-010-0543-5
  23. Noctor G, Foyer CH. Ascorbate and glutathione: keeping active oxygen under control. Annu Review Plant Biol 1998;49(1):249-79. https://doi.org/10.1146/annurev.arplant.49.1.249
  24. Zaefyzadeh M, Quliyev RA, Babayeva SM, Abbasov MA. The effect of the interaction between genotypes and drought stress on the superoxide dismutase and chlorophyll content in durum wheat landraces. Turkish J Biol 2009;33(1):1-7.
  25. A-H-Mackerness S, John CF, Jordan B, Thomas B. Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Lett 2001;489(2-3):237-42. https://doi.org/10.1016/S0014-5793(01)02103-2
  26. Herrera-Vasquez A, Salinas P, Holuigue L. Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front Plant Sci 2015:6.
  27. Joo JH, Wang S, Chen J, Jones A, Fedoroff NV. Different signaling and cell death roles of heterotrimeric G protein a and b subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 2005;17(3):957-70. https://doi.org/10.1105/tpc.104.029603
  28. Mammarella ND, Cheng Z, Fu ZQ, Daudi A, Bolwell GP, Dong X, Ausubel FM. Apoplastic peroxidases are required for salicylic acid-mediated defense against Pseudomonas syringae. Phytochemistry 2015;112:110-21. https://doi.org/10.1016/j.phytochem.2014.07.010
  29. O'Brien JA, Daudi A, Finch P, Butt VS, Whitelegge JP, Souda P, Ausubel FM, Bolwell GP. A peroxidase-dependent apoplastic oxidative burst in cultured Arabidopsis cells functions in MAMP-elicited defense. Plant Physiol 2012;158(4):2013-27. https://doi.org/10.1104/pp.111.190140
  30. Torres MA, Dangl JL, Jones JD. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 2002;99(1):517-22. https://doi.org/10.1073/pnas.012452499
  31. Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F. Interplay between MAMPtriggered and SA-mediated defense responses. Plant J 2008;53(5):763-75. https://doi.org/10.1111/j.1365-313X.2007.03369.x
  32. Wrzaczek M, Brosche M, Kangasjarvi J. ROS signaling loopsdproduction, perception, regulation. Curr Opin Plant Biol 2013;16(5):575-82. https://doi.org/10.1016/j.pbi.2013.07.002
  33. Ali MB, Yu K-W, Hahn E-J, Paek K-Y. Methyl jasmonate and salicylic acid elicitation induces ginsenosides accumulation, enzymatic and non-enzymatic antioxidant in suspension culture Panax ginseng roots in bioreactors. Plant Cell Rep 2006;25(6):613-20. https://doi.org/10.1007/s00299-005-0065-6
  34. de Costa F, Yendo ACA, Fleck JD, Gosmann G, Fett-Neto AG. Accumulation of a bioactive triterpene saponin fraction of Quillaja brasiliensis leaves is associated with abiotic and biotic stresses. Plant Physiol Biochem 2013;66:56-62. https://doi.org/10.1016/j.plaphy.2013.02.003
  35. Hu X, Neill S, Cai W, Tang Z. Hydrogen peroxide and jasmonic acid mediate oligogalacturonic acid-induced saponin accumulation in suspension-cultured cells of Panax ginseng. Physiol Plant 2003;118(3):414-21. https://doi.org/10.1034/j.1399-3054.2003.00124.x
  36. Kang S-M, Min J-Y, Kim Y-D, Kang Y-M, Park D-J, Jung H-N, Jung H-N, Kim S-W. Effects of methyl jasmonate and salicylic acid on the production of bilobalide and ginkgolides in cell cultures of Ginkgo biloba. Vitro Cell Dev Biol Plant 2006;42(1):44-9. https://doi.org/10.1079/IVP2005719
  37. Mehdy MC. Active oxygen species in plant defense against pathogens. Plant Physiol 1994;105(2):467. https://doi.org/10.1104/pp.105.2.467
  38. Tewari RK, Paek K-Y. Salicylic acid-induced nitric oxide and ROS generation stimulate ginsenoside accumulation in Panax ginseng roots. J Plant Growth Regul 2011;30(4):396-404. https://doi.org/10.1007/s00344-011-9202-3
  39. Zhao J, Davis LC, Verpoorte R. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 2005;23(4):283-333. https://doi.org/10.1016/j.biotechadv.2005.01.003
  40. Attele AS, Wu JA, Yuan C-S. Ginseng pharmacology: multiple constituents and multiple actions. Biochem Pharmacol 1999;58(11):1685-93. https://doi.org/10.1016/S0006-2952(99)00212-9
  41. Kennedy DO, Scholey AB. Ginseng: potential for the enhancement of cognitive performance and mood. Pharmacol Biochem Behav 2003;75(3):687-700. https://doi.org/10.1016/S0091-3057(03)00126-6
  42. Leung KW, Wong AS-T. Pharmacology of ginsenosides: a literature review. Chin Med 2010;5(1):20. https://doi.org/10.3760/cma.j.issn.1673-4777.2010.01.009
  43. Lu J-M, Yao Q, Chen C. Ginseng compounds: an update on their molecular mechanisms and medical applications. Curr Vasc Pharmacol 2009;7(3):293-302. https://doi.org/10.2174/157016109788340767
  44. Production of antioxidant compounds by culture of Panax ginseng CA Meyer hairy roots. In: Jeong G-T, Park D-H, Ryu H-W, Hwang B, Woo J-C, Kim D, Kim SW, editors. Twenty-sixth Symposium on Biotechnology for Fuels and Chemicals. Springer; 2005.
  45. Rahman M, Punja ZK. Factors influencing development of root rot on ginseng caused by Cylindrocarpon destructans. Phytopathology 2005;95(12):1381-90. https://doi.org/10.1094/PHYTO-95-1381
  46. Reeleder R, Brammall R. Pathogenicity of Pythium species, Cylindrocarpon destructans, and Rhizoctonia solani to ginseng seedlings in Ontario. Can J Plant Pathol 1994;16(4):311-6. https://doi.org/10.1080/07060669409500736
  47. Farh ME-A, Kim Y-J, Singh P, Yang D-C. Cross interaction between Ilyonectria mors-panacis isolates infecting Korean ginseng and ginseng saponins in correlation with their pathogenicity. Phytopathology 2017;107(5):561-9. https://doi.org/10.1094/PHYTO-05-16-0210-R
  48. Liu J, Wang Q, Sun M, Zhu L, Yang M, Zhao Y. Selection of reference genes for quantitative real-time PCR normalization in Panax ginseng at different stages of growth and in different organs. PloS One 2014;9(11):e112177. https://doi.org/10.1371/journal.pone.0112177
  49. Kim Y-J, Jeon J-N, Jang M-G, Oh JY, Kwon W-S, Jung S-K, Yang DC. Ginsenoside profiles and related gene expression during foliation in Panax ginseng Meyer. J Ginseng Res 2014;38(1):66-72. https://doi.org/10.1016/j.jgr.2013.11.001
  50. Pan X, Welti R, Wang X. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 2010;5(6):986. https://doi.org/10.1038/nprot.2010.37
  51. Brennan T, Frenkel C. Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol 1977;59(3):411-6. https://doi.org/10.1104/pp.59.3.411
  52. Oh J-Y, Kim Y-J, Jang M-G, Joo S, Kwon W-S, Kim S-Y, Jung S-K, Yang D-C. Investigation of ginsenosides in different tissues after elicitor treatment in Panax ginseng. J Ginseng Res 2014;38(4):270-7. https://doi.org/10.1016/j.jgr.2014.04.004
  53. Rahimi S, Kim Y-J, Sukweenadhi J, Zhang D, Yang D-C. PgLOX6 encoding a lipoxygenase contributes to jasmonic acid biosynthesis and ginsenoside production in Panax ginseng. J Exp Bot 2016;67(21):6007-19. https://doi.org/10.1093/jxb/erw358
  54. Gust AA, Nurnberger T. Plant immunology: a life or death switch. Nature 2012;486(7402):198-9. https://doi.org/10.1038/486198a
  55. Ashry NA, Mohamed HI. Impact of secondary metabolites and related enzymes in flax resistance and or susceptibility to powdery mildew. WJAS 2011;7(1):78-85.
  56. Radwan DEM, Fayez KA, Mahmoud SY, Lu G. Modifications of Antioxidant Activity and Protein Composition of Bean Leaf Due to Bean Yellow Mosaic Virus Infection and Salicylic Acid Treatments. Acta Physiol Plant 2010;32(5):891-904. https://doi.org/10.1007/s11738-010-0477-y
  57. Bilski P, Li M, Ehrenshaft M, Daub M, Chignell C. Symposium-in-Print vitamin B6 (pyridoxine) and its derivatives are efficient singlet oxygen quenchers and potential fungal antioxidants. Photochem Photobiol 2000;71(2):129-34. https://doi.org/10.1562/0031-8655(2000)0710129SIPVBP2.0.CO2
  58. Affek HP, Yakir D. Protection by isoprene against singlet oxygen in leaves. Plant Physiol 2002;129(1):269-77. https://doi.org/10.1104/pp.010909
  59. Balestrazz A, Macovei A, Tava A, Avato P, Raimondi E, Carbonera D. Unraveling the response of plant cells to cytotoxic saponins: role of metallothionein and nitric oxide. Plant Signal Behav 2011;6(4):516-9. https://doi.org/10.4161/psb.6.4.14746
  60. Loreto F, Mannozzi M, Maris C, Nascetti P, Ferranti F, Pasqualini S. Ozone quenching properties of isoprene and its antioxidant role in leaves. Plant Physiol 2001;126(3):993-1000. https://doi.org/10.1104/pp.126.3.993

Cited by

  1. Silicon confers protective effect against ginseng root rot by regulating sugar efflux into apoplast vol.9, pp.1, 2019, https://doi.org/10.1038/s41598-019-54678-x
  2. Comprehensive Genome Analysis on the Novel Species Sphingomonas panacis DCY99 T Reveals Insights into Iron Tolerance of Ginseng vol.21, pp.6, 2020, https://doi.org/10.3390/ijms21062019
  3. Implications of the Human Gut-Brain and Gut-Cancer Axes for Future Nanomedicine vol.14, pp.11, 2020, https://doi.org/10.1021/acsnano.0c07258
  4. Rhizoplane and Rhizosphere Fungal Communities of Geographically Isolated Korean Bellflower (Campanula takesimana Nakai) vol.10, pp.2, 2020, https://doi.org/10.3390/biology10020138
  5. Cumulative Production of Bioactive Rg3, Rg5, Rk1, and CK from Fermented Black Ginseng Using Novel Aspergillus niger KHNT-1 Strain Isolated from Korean Traditional Food vol.9, pp.2, 2020, https://doi.org/10.3390/pr9020227
  6. Ginsenosides Conversion and Anti-Oxidant Activities in Puffed Cultured Roots of Mountain Ginseng vol.9, pp.12, 2020, https://doi.org/10.3390/pr9122271
  7. The history, etiology, and management of ginseng replant disease: a Canadian perspective in review vol.101, pp.6, 2020, https://doi.org/10.1139/cjps-2021-0106