DOI QR코드

DOI QR Code

Cylindrocarpon destructans/Ilyonectria radicicola-species complex: Causative agent of ginseng root-rot disease and rusty symptoms

  • Farh, Mohamed El-Agamy (Graduate School of Biotechnology and Ginseng Bank, College of Life Science, Kyung Hee University) ;
  • Kim, Yeon-Ju (Department of Oriental Medicinal Biotechnology, College of Life Sciences, Kyung Hee University) ;
  • Kim, Yu-Jin (Department of Oriental Medicinal Biotechnology, College of Life Sciences, Kyung Hee University) ;
  • Yang, Deok-Chun (Graduate School of Biotechnology and Ginseng Bank, College of Life Science, Kyung Hee University)
  • Received : 2016.09.08
  • Accepted : 2017.01.02
  • Published : 2018.01.15

Abstract

Cylindrocarpon destructans/Ilyonectria radicicola is thought to cause both rusty symptom and root-rot disease of American and Korean ginseng. Root-rot disease poses a more serious threat to ginseng roots than rusty symptoms, which we argue result from the plant defense response to pathogen attack. Therefore, strains causing rotten root are characterized as more aggressive than strains causing rusty symptoms. In this review, we state 1- the molecular evidence indicating that the root-rot causing strains are genetically distinct considering them as a separate species of Ilyonectria, namely I. mors-panacis and 2- the physiological and biochemical differences between the weakly and highly aggressive species as well as those between rusty and rotten ginseng plants. Eventually, we postulated that rusty symptom occurs on ginseng roots due to incompatible interactions with the weakly aggressive species of Ilyonectria, by the established iron-phenolic compound complexes while root-rot is developed by I. morspanacis infection due to the production of high quantities of hydrolytic and oxidative fungal enzymes which destroy the plant defensive barriers, in parallel with the pathogen growth stimulation by utilizing the available iron. Furthermore, we highlight future areas for study that will help elucidate the complete mechanism of root-rot disease development.

Keywords

References

  1. Kim YJ, Jeon JN, Jang MG, Oh JY, Kwon WS, Jung SK, Yang DC. Ginsenoside profiles and related gene expression during foliation in Panax ginseng Meyer. J Ginseng Res 2013;38:66-72.
  2. Leung KW, Wong AS. Pharmacology of ginsenosides: a literature review. Chin Med 2010;5:20. http://dx.doi.org/10.1186/1749-8546-5-20.
  3. Wen J, Zimmer EA. Phylogeny and biogeography of Panax L. (the ginseng genus, Araliaceae): inferences from ITS sequences of nuclear ribosomal DNA. Mol Phylogenet Evol 1996;6:167-77. https://doi.org/10.1006/mpev.1996.0069
  4. Choi HK, Wen L. A phylogenetic analysis of Panax (Araliaceae): Integrating cpDNA restriction site and nuclear rDNA ITS sequence data. Plant Syst Evol 2000;224:109-20. https://doi.org/10.1007/BF00985269
  5. Attele AS, Wu JA, Yuan CS. Ginseng pharmacology: multiple constituents and multiple actions. Biochem Pharmacol 1999;58:1685-93. https://doi.org/10.1016/S0006-2952(99)00212-9
  6. Kennedy DO, Scholey AB. Ginseng: potential for the enhancement of cognitive performance and mood. Pharmacol Biochem Behav 2003;75:687-700. https://doi.org/10.1016/S0091-3057(03)00126-6
  7. Lu JM, Yao Q, Chen C. Ginseng compounds: an update on their molecular mechanisms and medical applications. Curr Vasc Pharmacol 2009;7:293-302. https://doi.org/10.2174/157016109788340767
  8. Proctor JTA, Bailey WG. Ginseng: Industry, botany and culture. Hortic Rev 1987;9:187-236.
  9. 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. Korea Ginseng and Tobacco Research Inst.; 1992. p. 121-84.
  10. Yu YH, Ohh SH. Research on ginseng diseases in Korea. Korean J Ginseng Sci 1993;17:61-8.
  11. Ziezold M, Reeleder RD, Hall R, Proctor JTA. Effect of drenching soil with benomyl, propiconazole, and fluazinam on incidence of disappearing root rot of ginseng. J Ginseng Res 1998;22:237-43.
  12. Howard RJ, Garland JA, Seaman WL. Diseases and pests of vegetable crops in Canada: an illustrated compendium. Entomological Society of Canada & Canadian Phytopathological Society; 1994.
  13. Putnam ML, du Toit LJ. First report of Alternaria blight caused by Alternaria panax on ginseng (Panax quinquefolius) in Oregon and Washington, USA. Plant Pathol 2003;52:406. https://doi.org/10.1046/j.1365-3059.2003.00828.x
  14. Kim YC, Lee JH, Bae YS, Sohn BK, Park SK. Development of effective environmentally-friendly approaches to control Alternaria blight and anthracnose diseases of Korean ginseng. Eur J Plant Pathol 2010;127:443-50. https://doi.org/10.1007/s10658-010-9610-4
  15. Cho H-S, Jeon Y-H, Do G-R, Cho D-H, Yu Y-H. Mycological characteristics of Botrytis cinerea causing gray mold on ginseng in Korea. J Ginseng Res 2008;32: 26-32. https://doi.org/10.5142/JGR.2008.32.1.026
  16. Takimoto S. Colletotrichum panacicola Uyeda and Takimoto. Chosen Nokwai ho 1919;14:24-5 (In Japanase).
  17. Chung HS, Bae HW. Ginseng anthracnose in Korea: Factors affecting primary inoculum, growth of the pathogen, disease development and control. Korean J Plant Prot 1979;18:35-41.
  18. Darmono TW, Owen ML, Parke JL. Isolation and pathogenicity of Phytophthora cactorum from forest and ginseng garden soils in Wisconsin. Plant Dis 1991;75(6):610-2. https://doi.org/10.1094/PD-75-0610
  19. Bobev SG, Baeyen S, Crepel C, Maes M. First report of Phytophthora cactorum on American ginseng (Panax quinquefolius) in Bulgaria. Plant Dis 2003;87:752.
  20. Hill SN, Hausbeck, MK. Virulence and fungicide sensitivity of Phytophthora cactorum isolated from American ginseng gardens in Wisconsin and Michigan 2008;92:1183-1189. https://doi.org/10.1094/PDIS-92-8-1183
  21. Reeleder RD, Brammall RA. Pathogenicity of Pythium species, Cylindrocarpon destructans, and Rhizoctonia solani to ginseng seedlings in Ontario. Can J Plant Pathol 1994;16:311-6. https://doi.org/10.1080/07060669409500736
  22. Hildebrand AA. Root rot of ginseng in Ontario caused by members of the genus Ramularia. Can J Res 1935;12:82-114. https://doi.org/10.1139/cjr35-007
  23. Reeleder RD, Roy R, Capell B. Seed and root rots of ginseng (Panax quinquefolius L) caused by Cylindrocarpon destructans and Fusarium spp. J Ginseng Res 2002;26:151-8. https://doi.org/10.5142/JGR.2002.26.3.151
  24. Rahman M, Punja ZK. Biochemistry of ginseng root tissues affected by rusty root symptoms 2005;43:1103-1114. https://doi.org/10.1016/j.plaphy.2005.09.004
  25. Rahman M, Punja ZK. Factors influencing development of root rot on ginseng caused by Cylindrocarpon destructans. Phytopathology 2005;95:1381-90. https://doi.org/10.1094/PHYTO-95-1381
  26. Cabral A, Groenewald JZ, Rego C, Oliveira H, Crous PW. Cylindrocarpon root rot: multi-gene analysis reveals novel species within the Ilyonectria radicicolaspecies complex. Mycol Prog 2012;11:655-88. https://doi.org/10.1007/s11557-011-0777-7
  27. Zinnsmeister CL. Ramularia root-rots of ginseng. Phytopathology 1918;8:557-71.
  28. Chung HS. Ginseng disease. Research reports of the Korean Society of Plant Protection. Seoul: Korean Society of Plant Protection; 1979. p. 107-44.
  29. Punja ZK, Wan A, Goswami RS. Root rot and distortion of ginseng seedling roots caused by Fusarium oxysporum. Can J Plant Pathol 2008;30:565-74. https://doi.org/10.1080/07060660809507556
  30. Wollenweber HW. Ramularia, Mycosphaerella, Nectria, Calonectria. Phytopathology 1913;3:197-242.
  31. Booth C. The genus Cylindrocarpon. Myc Papers 1966;104:1-56.
  32. Samuels GJ, Brayford D. Variation in Nectria radicicola and its anamorph, Cylindrocarpon destructans. Mycol Res 1990;94:433-42. https://doi.org/10.1016/S0953-7562(10)80001-2
  33. Rossman AY, Samuels GJ, Rogerson CT, Lowen R. Genera of the Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Stud Mycol 1999;42:1-248.
  34. Mantiri FR, Samuels GJ, Rahe JE, Honda BM. Phylogenetic relationships in Neonectria species having Cylindrocarpon anamorphs inferred from mitochondrial ribosomal DNA sequences. Can J Bot 2001;79:334-40.
  35. Brayford D, Honda BM, Mantiri FR, Samuels GJ. Neonectria and Cylindrocarpon: the Nectria mammoidea group and species lacking microconidia. Mycologia 2004;96:572-97. https://doi.org/10.1080/15572536.2005.11832955
  36. Booth C. Studies of pyrenomycetes. IV. Nectria (part 1). Myc Papers 1959;73: 1-115.
  37. Samuels GJ, Brayford D. Species of Nectria (sensu lato). with red perithecia and striate ascospores. Sydowia 1994;46:75-161.
  38. Brayford D, Samuels GJ. Some didymosporous species of Nectria with nonmicroconidial Cylindrocarpon anamorphs. Mycologia 1993;85:612-37. https://doi.org/10.2307/3760508
  39. Chaverri P, Salgado C, Hirooka Y, Rossman AY, Samuels GJ. Delimitation of Neonectria and Cylindrocarpon (Nectriaceae, Hypocreales, Ascomycota) and related genera with Cylindrocarpon like anamorphs. Stud Mycol 2011;68:57-78. https://doi.org/10.3114/sim.2011.68.03
  40. Booth C. Nectria radicicola. C.M.I. Descriptions of Pathogenic Fungi and Bacteria 1967;148:1-2.
  41. Crous PW, Slippers B, Wingfield MJ, Rheeder J, Marasas WFO, Philips AJL, Alves A, Burgess T, Barber P, Groenewald JZ. Phylogenetic lineages in the Botryosphaeriaceae. Stud Mycol 2006;55:235-53. https://doi.org/10.3114/sim.55.1.235
  42. Crous PW, Schoch CL, Hyde KD, Wood AR, Gueidan C, de Hoog GS, Groenewald JZ. Phylogenetic lineages in the Capnodiales. Stud Mycol 2009;64:17-47. https://doi.org/10.3114/sim.2009.64.02
  43. Grafenhan T, Schroers H-J, Nirenberg HI, Seifert KA. An overview of the taxonomy, phylogeny, and typification of nectriaceous fungi in Cosmospora, Acremonium, Fusarium, Stilbella, and Volutellax. Stud Mycol 2011;68:79-113. https://doi.org/10.3114/sim.2011.68.04
  44. Lombard L, Crous PW, Wingfield BD, Wingfield MJ. Phylogeny and systematics of the genus Calonectria. Stud Mycol 2010;66:31-69. https://doi.org/10.3114/sim.2010.66.03
  45. Schroers H-J, Grafenhan T, Nirenberg HI, Seifert KA. A revision of Cyanonectria and Geejayessia gen. nov., and related species with Fusarium-like anamorphs. Stud Mycol 2011;68:115-38. https://doi.org/10.3114/sim.2011.68.05
  46. Lee C, Kim KY, Lee JE, Kim S, Ryu D, Choi JE, An G. Enzymes hydrolyzing structural components and ferrous ion cause rusty-root symptom on ginseng (Panax ginseng). J Microbiol Biotechnol 2011;21:192-6. https://doi.org/10.4014/jmb.1008.08010
  47. Seifert KA, McMullen CR, Yee D, Reeleder RD, Dobinson KF. Molecular differentiation and detection of ginseng-adapted isolates of the root rot fungus Cylindrocarpon destructans. Phytopathology 2003;93:1533-42. https://doi.org/10.1094/PHYTO.2003.93.12.1533
  48. Lee SS. Korean ginseng (ginseng cultivation), Korean ginseng and T. Research institute 2007;18-40.
  49. Hankins A. Producing and Marketing Wild Simulated Ginseng in Forest and Agroforestry Systems. Produced by Communications and Marketing, College of Agriculture and Life Sciences, Virginia Polytechnic Institute and State University; 2009.
  50. Rahman M, Punja ZK. Influence of iron on Cylindrocarpon root rot development on ginseng. Phytopathology 2006;96:1179-87. https://doi.org/10.1094/PHYTO-96-1179
  51. Stoltz LP. Mineral nutrition studies of American ginseng. Lexington: Ky: In Pro. 4th Natl. Ginseng Conf.; 1982.
  52. Kim JH, Kim SG, Kim MS, Jeon YH, Cho DH, Kim YH. Different structural modifications associated with development of ginseng root rot caused by Cylindrocarpon destructans. Plant Pathol J 2009;25:1-5. https://doi.org/10.5423/PPJ.2009.25.1.001
  53. Yang D-C, Kim Y-H, Yun K-Y, Lee S-S, Kwon J-N, Kang H-M. Red-colored phenomena of ginseng (Panax ginseng C. A. Meyer): root and soil environment. J Ginseng Sci 1997;21:91-7.
  54. Punja ZK, Wan A, Goswami RS, Verma N, Rahman M, Barasubiye T, Seifert KA, Levesque CA. Diversity of Fusarium species associated with discolored ginseng roots in British Columbia. Can J Plant Pathol 2007;29:340-53. https://doi.org/10.1080/07060660709507480
  55. Reeleder RD, Hoke SMT, Zhang Y. Rusted root of ginseng (Panax quinquefolius) is caused by a species of Rhexocercosporidium. Phytopathology 2006;96:1243-54. https://doi.org/10.1094/PHYTO-96-1243
  56. Choi JE, Ryuk JA, Kim JH, Choi CH, Chun JS, Kim YJ, Lee HB. Identification of endophytic bacteria isolated from rusty-colored root of Korean ginseng (Panax ginseng) and its induction. Korean J Med Crop Sci 2005;13:1-5.
  57. Pathrose B, Jones EE, Jaspers MV, Ridgway HJ. High genotypic and virulence diversity in Ilyonectria liriodendri isolates associated with black foot disease in New Zealand vineyards. Plant Pathol 2014;63:613-24. https://doi.org/10.1111/ppa.12140
  58. Crombie WML, Crombie L, Green JB, Lucas JA. Pathogenicity of the take all fungus to oats: its relationship to the concentration and detoxification of the four avenacins. Phytochemistry 1986;25:2075-83. https://doi.org/10.1016/0031-9422(86)80069-3
  59. Fewell AM, Roddick JG. Interactive antifungal activity of the glycoalkaloid solanine and chaconine. Phytochemistry 1993;33:323-8. https://doi.org/10.1016/0031-9422(93)85511-O
  60. Morrissey JP, Osbourn AE. Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol Mol Biol Rev 1999;63:708-24.
  61. Papadopoulou K, Melton RE, Leggett M, Daniels MJ, Osbourn AE. Compromised disease resistance in saponin-deficient plants. Proc Natl Acad Sci 1999;96:12923-8. https://doi.org/10.1073/pnas.96.22.12923
  62. Nicol RW, Traquair JA, Bernards MA. Ginsenosides as host resistance factors in American ginseng (Panax quinquefolius). Can J Bot 2002;80:557-62. https://doi.org/10.1139/b02-034
  63. Osbourn A. Saponins and plant defence - a soap story. Trends in Plant Sci 1996;1:4-9. https://doi.org/10.1016/S1360-1385(96)80016-1
  64. Yousef LF, Bernards MA. In vitro metabolism of ginsenosides by the ginseng root pathogen Pythium irregulare. Phytochemistry 2006;67(16):1740-9. https://doi.org/10.1016/j.phytochem.2005.06.030
  65. Nicol RW, Yousef L, Traquair JA, Bernards MA. Ginsenosides stimulate the growth of soilborne pathogens of American ginseng. Phytochemistry 2003;64:257-64. https://doi.org/10.1016/S0031-9422(03)00271-1
  66. Ivanov DA, Bernards MA. Ginsenosidases and the pathogenicity of Pythium irregulare. Phytochemistry 2012;78:44-53. https://doi.org/10.1016/j.phytochem.2012.02.024
  67. Shah K, Kumar RG, Verma S, Dubey RS. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 2001;161:1135-44. https://doi.org/10.1016/S0168-9452(01)00517-9
  68. Sharma P, Dubey RS. Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep 2007;26:2027-38. https://doi.org/10.1007/s00299-007-0416-6
  69. 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;2012:26.
  70. 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:e1002185. https://doi.org/10.1371/journal.ppat.1002185
  71. Hemetsberger C, Herrberger C, Zechmann B, Hillmer M, Doehlemann G. The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog 2012;8:e1002684. https://doi.org/10.1371/journal.ppat.1002684

Cited by

  1. The Effect of Fungicides on Mycelial Growth and Conidial Germination of the Ginseng Root Rot Fungus, Cylindrocarpon destructans vol.45, pp.3, 2018, https://doi.org/10.5941/myco.2017.45.3.220
  2. Effect of the biocontrol bacterium Bacillus amyloliquefaciens on the rhizosphere in ginseng plantings vol.21, pp.3, 2018, https://doi.org/10.1007/s10123-018-0015-0
  3. Diversity and antifungal activity of endophytic bacteria associated with Panax ginseng seedlings vol.12, pp.6, 2018, https://doi.org/10.1007/s11816-018-0504-9
  4. Fungal Endophytes of Populus trichocarpa Alter Host Phenotype, Gene Expression, and Rhizobiome Composition vol.32, pp.7, 2019, https://doi.org/10.1094/mpmi-05-18-0133-r
  5. 녹비작물 토양환원과 태양열 소독에 의한 3년생 인삼의 뿌리썩음병 억제효과 vol.27, pp.4, 2018, https://doi.org/10.7783/kjmcs.2019.27.4.284
  6. 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
  7. Purification and Characterization of a Novel Antifungal Flagellin Protein from Endophyte Bacillus methylotrophicus NJ13 against Ilyonectria robusta vol.7, pp.12, 2018, https://doi.org/10.3390/microorganisms7120605
  8. Different Age-Induced Changes in Rhizosphere Microbial Composition and Function of Panax ginseng in Transplantation Mode vol.11, pp.None, 2020, https://doi.org/10.3389/fpls.2020.563240
  9. Metabolomic Profiling of Fungal Pathogens Responsible for Root Rot in American Ginseng vol.10, pp.1, 2018, https://doi.org/10.3390/metabo10010035
  10. Microbial Community Changes in the Rhizosphere Soil of Healthy and Rusty Panax ginseng and Discovery of Pivotal Fungal Genera Associated with Rusty Roots vol.2020, pp.None, 2020, https://doi.org/10.1155/2020/8018525
  11. Comprehensive Genome Analysis on the Novel Species Sphingomonas panacis DCY99 T Reveals Insights into Iron Tolerance of Ginseng vol.21, pp.6, 2018, https://doi.org/10.3390/ijms21062019
  12. Whole-genome and time-course dual RNA-Seq analyses reveal chronic pathogenicity-related gene dynamics in the ginseng rusty root rot pathogen Ilyonectria robusta vol.10, pp.None, 2018, https://doi.org/10.1038/s41598-020-58342-7
  13. The Effect of Biopreparations and Biostimulants on the Chemical Composition and Microorganisms Associated with Verticillium Wilt of Horseradish Roots (Armoracia rusticana Gaertn.) vol.11, pp.2, 2018, https://doi.org/10.3390/app11020680
  14. Identification of N,N',N"-triacetylfusarinine C as a key metabolite for root rot disease virulence in American ginseng vol.45, pp.1, 2018, https://doi.org/10.1016/j.jgr.2019.08.008
  15. Antagonistic effect of Frankia F1 on Ginseng crops soil-borne diseases and microbial community soil structure vol.31, pp.5, 2018, https://doi.org/10.1080/09583157.2020.1867708
  16. Production of Siderophores by an Apple Root-Associated Streptomyces ciscaucasicus Strain GS2 Using Chemical and Biological OSMAC Approaches vol.26, pp.12, 2021, https://doi.org/10.3390/molecules26123517
  17. Alteration of the Soil Microbiota in Ginseng Rusty Roots: Application of Machine Learning Algorithm to Explore Potential Biomarkers for Diagnostic and Predictive Analytics vol.69, pp.29, 2018, https://doi.org/10.1021/acs.jafc.1c01314
  18. Root rot-infected Sanqi ginseng rhizosphere harbors dynamically pathogenic microbiotas driven by the shift of phenolic acids vol.465, pp.1, 2018, https://doi.org/10.1007/s11104-021-05034-4
  19. Effect of Seed Dressing and Soil Chemical Properties on Communities of Microorganisms Associated with Pre-Emergence Damping-Off of Broad Bean Seedlings vol.11, pp.9, 2021, https://doi.org/10.3390/agronomy11091889
  20. Endophytic fungi stimulate the concentration of medicinal secondary metabolites in houttuynia cordata thunb vol.16, pp.9, 2018, https://doi.org/10.1080/15592324.2021.1929731
  21. The discovery of pivotal fungus and major determinant factor shaping soil microbial community composition associated with rot root of American ginseng vol.16, pp.11, 2021, https://doi.org/10.1080/15592324.2021.1952372
  22. Allyl Isothiocyanate in the Volatiles of Brassica juncea Inhibits the Growth of Root Rot Pathogens of Panax notoginseng by Inducing the Accumulation of ROS vol.69, pp.46, 2018, https://doi.org/10.1021/acs.jafc.1c05225
  23. The comprehensive changes in soil properties are continuous cropping obstacles associated with American ginseng (Panax quinquefolius) cultivation vol.11, pp.1, 2021, https://doi.org/10.1038/s41598-021-84436-x
  24. Regulatory role of non-coding RNA in ginseng rusty root symptom tissue vol.11, pp.1, 2018, https://doi.org/10.1038/s41598-021-88709-3
  25. Metabolome and transcriptome analysis reveals the molecular profiles underlying the ginseng response to rusty root symptoms vol.21, pp.1, 2018, https://doi.org/10.1186/s12870-021-03001-w
  26. A simplified synthetic community rescues Astragalus mongholicus from root rot disease by activating plant-induced systemic resistance vol.9, pp.1, 2018, https://doi.org/10.1186/s40168-021-01169-9
  27. The history, etiology, and management of ginseng replant disease: a Canadian perspective in review vol.101, pp.6, 2018, https://doi.org/10.1139/cjps-2021-0106