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http://dx.doi.org/10.1016/j.jgr.2019.01.006

Taxonomy of fungal complex causing red-skin root of Panax ginseng in China  

Lu, Xiao H. (Biotechnology Research Center, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College)
Zhang, Xi M. (Biotechnology Research Center, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College)
Jiao, Xiao L. (Biotechnology Research Center, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College)
Hao, Jianjun J. (Department of Plant Science, School of Food and Agriculture, The University of Maine)
Zhang, Xue S. (Biotechnology Research Center, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College)
Luo, Yi (Biotechnology Research Center, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College)
Gao, Wei W. (Biotechnology Research Center, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College)
Publication Information
Journal of Ginseng Research / v.44, no.3, 2020 , pp. 506-518 More about this Journal
Abstract
Background: Red-skin root of Asian ginseng (Panax ginseng) significantly reduces the quality and limits the production of ginseng in China. The disease has long been thought to be a noninfectious physiological disease, except one report that proved it was an infectious disease. However, the causal agents have not been successfully determined. In the present study, we were to reveal the pathogens that cause red-skin disease. Methods: Ginseng roots with red-skin root symptoms were collected from commercial fields in Northeast China. Fungi were isolated from the lesion and identified based on morphological characters along with multilocus sequence analyses on internal transcription spacer, β-tubulin (tub2), histone H3 (his3), and translation elongation factor 1α (tef-1α). Pathogens were confirmed by inoculating the isolates in ginseng roots. Results: A total of 230 isolates were obtained from 209 disease samples. These isolates were classified into 12 species, including Dactylonectria sp., D. hordeicola, Fusarium acuminatum, F. avenaceum, F. solani, F. torulosum, Ilyonectria mors-panacis, I. robusta, Rhexocercosporidium panacis, and three novel species I. changbaiensis, I. communis, and I. qitaiheensis. Among them, I. communis, I. robusta, and F. solani had the highest isolation frequencies, being 36.1%, 20.9%, and 23.9%, respectively. All these species isolated were pathogenic to ginseng roots and caused red-skin root disease under appropriate condition. Conclusion: Fungal complex is the causal agent of red-skin root in P. ginseng.
Keywords
Cylindrocarpon; Fusarium; Ilyonectria; Panax ginseng; Root disease;
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1 Reeleder RD. Rhexocercosporidium panacis sp. nov., a new anamorphic species causing rusted root of ginseng (Panax quinquefolius). Mycologia 2007;99:91-8.   DOI
2 Reeleder RD, Brammall RA. Pathogenicity of Pythium species, Cylindrocarpon destructans, and Rhizoctonia solani to ginseng seedling in Onttario. Can J Plant Pathol 1994;16:311-6.   DOI
3 Lu XH, Jiao XL, Hao JJ, Chen AJ, Gao WW. Characterization of resistance to multiple fungicides in Botrytis cinerea populations from Asian ginseng in northeastern China. Eur J Plant Pathol 2016;144:467-76.   DOI
4 Crous PW, Verkleij GJM, Groenewald JZ, Samson RA. Fungal biodiversity. CBS Laboratory Manual Series 1. Utrecht: Centraalbureau voor Schimmelcultures; 2009.
5 Rayner RW. A mycological colour chart. Great Britain: Commonwealth Mycological Institute; 1970.
6 Nirenberg H. Untersuchungen uber die morphologische und biologische Differenzierung in der Fusarium-Sektion Liseola. Mitt Biol Bundesanst Land Forstwirtsch 1976;169:1-117.
7 White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, p. 315-22. In: Innis MA, Gelfand D, Sninsky JJ, White TJ, editors. PCR Protocols: a guide to methods and applications. San Diego: Academic Press; 1990.
8 Crous PW, Groenewald JZ, Risede JM, Simoneau P, Hywel-Jones NL. Calonectria species and their Cylindrocladium anamorphs: species with sphaeropedunculate vesicles. Stud Mycol 2004:415-30.   DOI
9 O'Donnell K, Kistler HC, Cigelnik E, Ploetz RC. Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. P Natl Acad Sci USA 1998;95:2044-9.   DOI
10 Santorum JM, Darriba D, Taboada GL, Posada D. jmodeltest.org: selection of nucleotide substitution models on the cloud. Bioinformatics 2014;30:1310-1.   DOI
11 Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 2008;75:758-71.   DOI
12 Cabral A, Rego C, Nascimento T, Oliveira H, Groenewald JZ, Crous PW. Multigene analysis and morphology reveal novel Ilyonectria species associated with black foot disease of grapevines. Fungal Biol 2012;116:62-80.   DOI
13 Ronquist F, Huelsenbeck JP. MrBayes version 3.0: Bayesian phylogenetic inference under mixed models. Bioinformatics 2013;19:1572-4.   DOI
14 Lu XH, Chen AJ, Zhang XS, Jiao XL, Gao WW. First report of Rhexocercosporidium panacis causing rusty root of Panax ginseng in Northeastern China. Plant Dis 2014;98:1580.
15 Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser D. Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 2000;31:21-32.   DOI
16 Song JY, Seo MW, Kim SI, Nam MH, Lim HS, Kim HG. Genetic diversity and pathogenicity of Cylindrocarpon destructans isolates obtained from Korean Panax ginseng. Mycobiology 2014;42:174-80.   DOI
17 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. Studies in Mycology 2011;68:57-78.   DOI
18 Aiello D, Guarnaccia V, Vitale A, Cirvilleri G, Granata G, Epifani F, Perrone G, Polizzi G, Groenewald JZ, Crous PW. Ilyonectria palmarum sp. nov. causing dry basal stem rot of Arecaceae. Eur J Plant Pathol 2014;138:347-59.   DOI
19 Lombard L, Bezuidenhout CM, Crous PW. Ilyonectria black foot rot associated with Proteaceae. Australas Plant Path 2013;42:337-49.   DOI
20 Lombard L, van Der Merwe NA, Groenewald JZ, Crous PW. Lineages in Nectriaceae: Re-evaluating the generic status of Ilyonectria and allied genera. Phytopathol Mediterranea 2014;53:515-32.
21 Lu XH, Jiao XL, Chen AJ, Luo Y, Gao WW. First report of Ilyonectria robusta causing rusty root of Asian ginseng in China. Plant Dis 2015;99:156.
22 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.   DOI
23 Farh MEA, Han JA, Kim YJ, Kim JC, Singh P, Yang DC. Discovery of a new primer set for detection and quantification of Ilyonectria mors-panacis in soils for ginseng cultivation. J Ginseng Res 2017.
24 Farh MEA, Kim YJ, Singh P, Yang DC. Cross interaction between Ilyonectriamors-panacis isolates infectingkorean ginseng and ginseng saponins in correlation with their pathogenicity. Phytopathology 2017;107:561-9.   DOI
25 Gao J, Wang Y, Guan YM, Chen CQ. Fusarium cerealis, a new pathogen causing ginseng (Panax ginseng) root rot in China. Plant Dis 2014;98:1433.   DOI
26 Guan YM, Lu BH, Wang Y, Gao J, Wu LJ. First report of root rot caused by Fusarium redolens on ginseng (Panax ginseng) in Jilin province of China. Plant Dis 2013;98:844.   DOI
27 Wang Y, Guan YM, Lu BH, Gao J. First report of ginseng (Panax ginseng) root rot caused by Fusarium acuminatum in China. Plant Dis 2015;100:525.   DOI
28 Aiello D, Polizzi G, Crous PW. Pleiocarpon gen. nov and a new species of Ilyonectria causing basal rot of Strelitzia reginae in Italy. IMA Fungus 2017;8:65-76.   DOI
29 Hu SY. A contribution to our knowledge of ginseng. Am J Chinese Med 1977;5:1-23.   DOI
30 Baranov A. Recent advances in our knowledge of the morphology, cultivation and uses of ginseng (Panax ginseng C.A. Meyer). Econ Bot 1966;20:403-6.   DOI
31 Zhou Y, Yang Z, Gao L, Liu W, Liu R, Zhao J, You J. Changes in element accumulation, phenolic metabolism, and antioxidative enzyme activities in the red-skin roots of Panax ginseng. J Ginseng Res 2017;41:307-15.   DOI
32 Yu YH, Ohh SH. Research on ginseng diseases in Korea. Korean J Ginseng Sci 1993;19:61-8.
33 Zhao Y, Li X, Hou Y. Biochemical changes in ginseng red coating root disease and comprehensive evaluation on the quality of disease roots. ACTA Phytopathol Sin 1997;27:175-9.
34 Liu J, Zhao Y, Liu B. A study on the anatomical and morphological characteristics of the ginseng roots infected by the red root disease. ACTA Phytopathol Sin 1998;28:72.
35 Wang Y. A preliminary study on cause of ginseng red skin disease in the second ginseng farm of Jinyu county. Spec Wild Econ Anim Plant Res 1963;2:9-15.
36 Shang Y, Chen Z, Si Y, Teng B. Research on the causes of red-skin disease of Panax ginseng. J Chinese Med Mater 1996;19:163-5.
37 Zhao Y. Recent progress on diagnosis and integrated management of ginseng rusty root disease in Northeast China. Spec Wild Econ Anim Plant Res 1998:41-6.
38 Wang Q, Jin R, Yun L, Wang J, Jiang X, Ma D, Bai Y. Occurrence investigation and pathogen study on ginseng rusty root rot. J Liaoning For Sci Technol 2014:15-7.
39 Li Z, Guo S, Tian S, Liu Z. Study on the causes for ginseng red skin sickness occurred in albic bed soil. ACTA Pedol Sin 1997;34:328-35.
40 Sun S, Li Y, Lu J, Jiao B, Jiang X. Soil geochemical characterics with ginseng red skin sickness in Ji'an city, Jilin province. J Jilin U 2010;40:412-6.
41 Wang Y, Li Z, Sun Y, Guo S, Tian S, Liu Z. Studies on the genesis of ginseng rust spots. Korean J Ginseng Sci 1997;21:69-77.
42 Farh MEA, Kim YJ, Kim YJ, Yang DC. Cylindrocarpon destructans/Ilyonectria radicicola-species complex: causative agent of ginseng root-rot disease and rusty symptoms. J Ginseng Res 2018;42:9-15.   DOI
43 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.   DOI
44 Cabral A, Groenewald JZ, Rego C, Oliveira H, Crous PW. Cylindrocarpon root rot: multi-gene analysis reveals novel species within the Ilyonectria radicicola species complex. Mycol Prog 2012;11:655-88.   DOI
45 Yan X. The comparative biology studies of Cylindrocarpon on ginseng and American ginseng. In: Plant pathology. Shenyang, China: Shenyang Agricultural University; 2002.
46 Sun J. The chemical induced resistant mechanism of Cylindrocarpon root rot of ginseng and molecular detection of Cylindrocarpon destructans. In: Pest and environment safety. China: Shenyang Agricultural University; 2013.
47 Wang S, Zhang A, Chen X, Lei F, Xu Y, Zhang L. Pesticides screening against ginseng root rust rot. Agrochemicals 2011;50:449-51.   DOI
48 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.   DOI
49 Punja ZK, Wan A, Rahman M. Role of Fusarium spp. in rusty-root development on ginseng in British Columbia. Can J Plant Pathol 2005;27:474.