Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2022-08-08
Page range: 256-268
Abstract views: 57
PDF downloaded: 2

Colletotrichum juglandis sp. nov. (Ascomycota: Glomerellaceae) associated with walnut leaf spot in China

Department of Plant Protection, College of Agriculture, Yangtze University, Jingzhou 434025, China
Department of Plant Protection, College of Agriculture, Yangtze University, Jingzhou 434025, China
Department of Plant Protection, College of Agriculture, Yangtze University, Jingzhou 434025, China
Animal and Plant Quarantine and Testing Center, Jingzhou 434020, China
Department of Plant Protection, College of Agriculture, Yangtze University, Jingzhou 434025, China
Department of Horticulture, College of Horticulture and Gardening, Yangtze University, Jingzhou 434025, China
Walnut (Juglans regia) Colletotrichum Phylogenetic analysis New species Taxonomy Fungi


Colletotrichum species are destructive pathogens, saprobes and endophytes on various plant hosts. However, the species occurring on walnut remains largely unresolved. Walnut leaf spot occurred seriously in orchards of Xingshan County, Hubei Province in China. To determine Colletotrichum spp. associated with Juglans regia, 22 isolates were obtained from the diseased leaf samples collected during 2019 and 2020. Seven isolates were further selected as representatives based on morphology and phylogeny using ITS, GAPDH, CHS-1 and ACT gene regions. The results revealed that the isolates belonged to two phylogenetic species complexes, C. gloeosporioides species complex (CGSC) comprising C. gloeosporioides and C. kahawae, and C. acutatum species complex (CASC) including C. nymphaeae, C. godetiae, C. fioriniae and a new species, namely Colletotrichum juglandis sp. nov.. Among them, C. kahawae was firstly reported from walnut.


<p>Abate, D., Pastore, C., Gerin, D., De Miccolis Angelini, R.M., Rotolo, C., Pollastro, S. &amp; Faretra, F. (2018) Characterization of <em>Monilinia</em> spp. populations on stone fruit in South Italy. <em>Plant Disease</em> 102: 1708–1717.&nbsp;</p>
<p>Abbasi, K., Abbasi, S., Fotouhifar, K.B., Zebarjadi, A.R. &amp; Cheghamirza, K. (2013) Genetic diversity of <em>Cytospora chrysosperma</em> isolates obtained from Iranian walnut trees using molecular markers. <em>African Journal of Biotechnology</em> 10: 15710–15716.&nbsp;</p>
<p>An, H. &amp; Yang, K. (2014) Resistance gene analogs in walnut (<em>Juglans regia</em>) conferring resistance to <em>Colletotrichum gloeosporioides</em>. <em>Euphytica</em> 197: 175–190.&nbsp;</p>
<p>Arx, J.A.V. (1957) Die arten der gattung <em>Colletotrichum</em> Cda. <em>Phytopathologische Zeitschrift</em> 29: 413–468.</p>
<p>Cai, L., Hyde, K.D., Taylor, P.W.J., Weir, B.S., Waller, J.M., Abang, M.M., Zhang, Z.J., Yang, Y.L., Phoulivong, S., Liu, Z.Y., Prihastuti, H., Shivas, R.G., McKenzie, E.H.C. &amp; Johnston, P.R. (2009) A polyphasic approach for studying <em>Colletotrichum</em>. <em>Fungal Diversity</em> 39: 183–204.&nbsp;</p>
<p>Cannon, P.F., Buddie, A.G. &amp; Bridge, P.D. (2008) The typification of <em>Colletotrichum gloeosporioides</em>. <em>Mycotaxon</em> 104: 189–204.</p>
<p>Cannon, P.F., Damm, U., Johnston, P.R. &amp; Weir, B.S. (2012) <em>Colletotrichum</em>–current status and future directions. <em>Studies in Mycology</em> 73: 181–213.&nbsp;</p>
<p>Carbone, I. &amp; Kohn, L.M. (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. <em>Mycologia</em> 91: 553–556.&nbsp;</p>
<p>Corda, A.C.I. (1831) Die Pilze Deutschlands.<em> In: </em>Sturm, J. (Ed.) Deutschlands Flora in Abbildungen nach der Natur mit Beschreibungen. Sturm, Nürnberg 3 (12): 33–64.</p>
<p>Crouch, J.A. (2014) <em>Colletotrichum caudatum</em> s. l. is a species complex. <em>IMA Fungus</em> 5: 17–30.&nbsp;</p>
<p>Crouch, J.A., Clarke, B.B. &amp; Hillman, B.I. (2009) What is the value of ITS sequence data in <em>Colletotrichum</em> systematics and species diagnosis? A case study using the falcate–spored graminicolous <em>Colletotrichum</em> group. <em>Mycologia</em> 101: 648–656.&nbsp;</p>
<p>Damm, U., Cannon, P.F., Woudenberg, J.H.C. &amp; Crous, P. (2012a) The <em>Colletotrichum acutatum</em> species complex. <em>Studies in Mycology</em> 73: 37–113.&nbsp;</p>
<p>Damm, U., Cannon, P.F., Woudenberg, J.H.C., Johnston, P.R., Weir, B.S., Tan, Y.P., Shivas, R.G. &amp; Crous, P.W. (2012b) The <em>Colletotrichum boninense</em> species complex. <em>Studies in Mycology</em> 73: 1–36.&nbsp;</p>
<p>Damm, U., Sato, T., Alizadeh, A., Groenewald, J.Z. &amp; Crous, P.W. (2019) The <em>Colletotrichum dracaenophilum</em>, <em>C. magnum</em> and <em>C. orchidearum</em> species complexes. <em>Studies in Mycology</em> 92: 1–46.&nbsp;</p>
<p>Damm, U., Woudenberg, J.H.C., Cannon, P.F. &amp; Crous, P.W. (2009) <em>Colletotrichum</em> species with curved conidia from herbaceous hosts. <em>Fungal Diversity</em> 39: 45–87.&nbsp;</p>
<p>Dean, R., Kan, J.A.L.V., Pretorius, Z.A., Hammond-Kosack, K.E., Di Pietro, A., Spanu, P.D., Rudd, J.J., Dickman, M., Kahmann, R., Ellis, J. &amp; Foster, G.D. (2012) The Top 10 fungal pathogens in molecular plant pathology. <em>Molecular Plant Pathology </em>13: 414–430.&nbsp; J.1364-3703.2011.00783.X</p>
<p>Doyle, V.P., Oudemans, P.V., Rehner, S.A. &amp; Litt, A. (2013) Habitat and host indicate lineage identity in <em>Colletotrichum gloeosporioides</em> s. l. from wild and agricultural landscapes in North America. <em>PLoS ONE</em> 8 (5): e62394.</p>
<p>Guerber, J.C., Liu, B., Correll, J.C. &amp; Johnston, P.R. (2003) Characterization of diversity in <em>Colletotrichum acutatum</em> <em>sensu lato</em> by sequence analysis of two gene introns, mtDNA and intron RFLPs, and mating compatibility. <em>Mycologia</em> 95: 872–895.</p>
<p>Hall, T.A. (1999) Bioedit: a user–friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. <em>Nucleic Acids Symposium Series</em> 41: 95–98.</p>
<p>He, L., Li, X., Gao, Y., Li, B., Mu, W. &amp; Liu, F. (2019) Characterization and fungicide sensitivity of <em>Colletotrichum</em> spp. from different hosts in Shandong, China. <em>Plant Disease</em> 103 (1): 34–43.&nbsp;</p>
<p>Jayawardena, R.S., Hyde, K.D., Damm, U., Cai, L., Liu, M., Li, X.H., Zhang, W., Zhao, W.S. &amp; Yang, J.Y. (2016) Notes on currently accepted species of <em>Colletotrichum</em>. <em>Mycosphere</em> 7 (8): 1192–1260.&nbsp;</p>
<p>Khan, A.A. &amp; Kundoo, A.A. (2018) Pests of walnut. <em>In:</em> <em>Pests and Their Management.</em> pp. 605–647.&nbsp;</p>
<p>Kumar, S., Stecher, G. &amp; Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. <em>Molecular Biology and Evolution</em> 33 (7): 1870–1874.&nbsp;</p>
<p>Lio, D.D., Cobo–Díaz, J.F., Masson, C., Chalopin, M., Kebe, D., Giraud, M., Verhaeghe, A., Nodet, P., Sarrocco, S. &amp; Floch, G.L. (2018) Combined metabarcoding and multi–locus approach for genetic characterization of <em>Colletotrichum</em> species associated with common walnut (<em>Juglans regia</em>) anthracnose in France. <em>Scientific Reports</em> 8: 10765.&nbsp;</p>
<p>Liu, F., Cai, L., Crous, P.W. &amp; Damm, U. (2014) The <em>Colletotrichum gigasporum</em> species complex. <em>Persoonia</em> 33: 83–97.&nbsp;</p>
<p>Liu, F., Wang, M., Damm, U., Crous, P.W. &amp; Cai, L. (2016) Species boundaries in plant pathogenic fungi: a <em>Colletotrichum</em> case study. <em>BMC Evolutionary Biology</em> 16: 81.&nbsp;</p>
<p>Liu, X.Y., Yao, J. &amp; Yang, J.X. (1995) A study on <em>Colletotrichum</em> classification of wooden plant in Shaanxi province. <em>Journal of Northwest Forestry College</em> 3: 29–30.</p>
<p>Marin–Felix, Y., Groenewald, J.Z., Cai, L., Chen, Q., Marincowitz, S., Barnes, I., Bensch, K., Braun, U., Camporesi, E., Damm, U., Beer, Z.W., Dissanayake, A., Edwards, J., Giraldo, A., Hernandez–Restrepo, M., Hyde, K.D., Jayawardena, R.S., Lombard, L., Luangsa-Ard, J., McTaggart, A.R., Rossman, A.Y., Sandoval–Denis, M., Shen, M., Shivas, R.G., Tan, Y.P., van der Linde, E.J., Wingfield, M.J., Wood, A.R., Zhang, J.Q., Zhang, Y. &amp; Crous, P.W. (2017) Genera of phytopathogenic fungi: GOPHY 1. <em>Studies in Mycology</em> 86: 99–216.&nbsp;</p>
<p>Mills, P.R., Hodson, A., Brown, A.E. (1992) Molecular differentiation of <em>Colletotrichum gloeosporioides</em> isolates infecting tropical fruits.<em> In: </em>Bailey, J.A. &amp; Jeger, M.J. (eds.)<em> Colletotrichum: Biology, Pathology and Control. </em>CABI, Wallingford, UK, pp. 269–288.</p>
<p>Mu, T., Zhang, Z., Liu, R., Liu, S., Li, Z., Zhang, X. &amp; Xia, J. (2021) Morphological and molecular phylogenetic analyses reveal three species of <em>Colletotrichum</em> in Shandong province, China. <em>MycoKeys</em> 85: 57–71.&nbsp;</p>
<p>Munir, M., Amsden, B., Dixon, E., Vaillancourt, L. &amp; Gauthier, N.A.W. (2016) Characterization of <em>Colletotrichum</em> species causing bitter rot of apple in Kentucky orchards. <em>Plant Disease</em> 100 (11): 2194–2203.&nbsp;</p>
<p>Nirenberg, H.I. (1976) Untersuchungen uber die morphologische und biologische differenzierung in der fusaium-sektion liseola. <em>Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft, Berlin-Dahlem</em> 169: 1–117.</p>
<p>Qu, W.W., Yang, K.Q., Liu, H.X. &amp; Hou, L.Q. (2011) Main diseases of walnut and integrated management in Shandong. <em>Plant Protection</em> 44: 136–140.&nbsp;</p>
<p>Quaedvlieg, W., Binder, M., Groenewald, J.Z., Summerell, B.A., Carnegie, A.J., Burgess, T.I., Crous, P.W. (2014) Introducing the consolidated species concept to resolve species in the <em>Teratosphaeriaceae</em>. <em>Persoonia</em> 33: 1–40.&nbsp;</p>
<p>Rambaut, A., Drummond, A. (2010) FigTree v.1.3.1. Institute of evolutionary biology, University of Edinburgh, Edinburgh, UK.</p>
<p>Ronquist, F., Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. <em>Bioinformatics</em> 19: 1572–1574.&nbsp;</p>
<p>Samarakoon, M.C., Peršoh, D., Hyde, K.D., Bulgakov, T.S., Manawasinghe, I.S., Jayawardena, R.S., Promputtha, I. (2018) <em>Colletotrichum acidae</em> sp. nov. from northern Thailand and a new record of <em>C. dematium</em> on Iris sp.. <em>Mycosphere</em> 9 (3): 583–597.&nbsp;</p>
<p>Sharma, G., Kumar, N., Weir, B.S., Hyde, K.D. &amp; Shenoy, B.D. (2013) The <em>ApMat</em> marker can resolve <em>Colletotrichum</em> species: a case study with <em>Mangifera indica</em>. <em>Fungal Diversity</em> 61: 117–138.&nbsp;</p>
<p>Squissato, V., Yucel, Y.H., Richardson, S.E., Alkhotani, A., Wong, D.T., Nijhawan, N. &amp; Chan, C.C. (2015) <em>Colletotrichum truncatum</em> species complex: treatment considerations and review of the literature for an unusual pathogen causing fungal keratitis and endophthalmitis. <em>Medical Mycology Case Reports</em> 9: 1–6.</p>
<p>Sreenivasaprasad, S., Brown, A.E. &amp; Mills, P.R. (1992) DNA sequence variation and interrelationship among <em>Colletotrichum</em> species causing strawberry anthracnose. <em>Physiological and Molecular</em> <em>Plant Pathology</em> 41: 265–281.&nbsp;</p>
<p>Stamatakis, A. (2014) RAxML Version 8: A tool for phylogenetic analysis and post–analysis of large phylogenies. Bioinformatics 30 (9): 1312–1313. btu033</p>
<p>Sutton, B.C. (1980) The Coelomycetes. Fungi Imperfecti with Pycnidia, Acervuli and Stromata. Commonwealth Mycological Institute, Kew, 696 pp.</p>
<p>Sutton, B.C. (1992) The genus Glomerella and its anamorph <em>Colletotrichum</em>. <em>In: Colletotrichum: Biology, Pathology, and Control. </em>CAB International, Wallingford, United Kingdom, 388 pp. [pp. 1–26.]</p>
<p>Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. &amp; Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. <em>Molecular Biology and Evolution</em> 28: 2731–2739.&nbsp;</p>
<p>Tan, X.D., Li, J.T., Bie, Z.R., Li, B.B. &amp; Shu, H.W. (2020) Investigation and thinking on the development of Xingshan Walnut industry. <em>Hubei Forestry Science and Technology</em> 49 (04): 83–86. [CNKI: SUN: FBLI.0.2020-04-023]</p>
<p>Than, P.P., Shivas, R.G., Jeewon, R., Pongsupasamit, S., Marney, T.S., Taylor, P.W.J., Hyde, K.D. (2008) Epitypification and phylogeny of <em>Colletotrichum acutatum</em> J.H. Simmonds. <em>Fungal Diversity</em> 28: 97–108.&nbsp;</p>
<p>Tibpromma, S., Hyde, K.D., Bhat, J.D., Mortimer, P.E., Xu, J., Promputtha, I., Doilom, M., Yang, J.B., Tang, A.M.C., Karunarathna, S.C. (2018) Identification of endophytic fungi from leaves of Pandanaceae based on their morphotypes and DNA sequence data from southern Thailand. <em>MycoKeys</em> 25–67.&nbsp;</p>
<p>Velho, A.C., Alaniz, S., Casanova, L., Mondino, P., Stadnik, M.J. &amp; Schoch, C. (2015) New insights into the characterization of <em>Colletotrichum</em> species associated with apple diseases in southern Brazil and Uruguay. <em>Fungal Biology</em> 119: 229–244.&nbsp;</p>
<p>Vieira, W.A.S., Lima, W.G., Nascimento, E.S., Michereff, S.J., Câmara, M.P.S. &amp; Doyle, V.P. (2017) The impact of phenotypic and molecular data on the inference of <em>Colletotrichum</em> diversity associated with <em>Musa</em>. <em>Mycologia</em> 109: 912–934.&nbsp;</p>
<p>Waller, J.M., Bridge, P.D., Black, R. &amp; Hakiza, G. (1993) Characterization of the coffee berry disease pathogen, <em>Colletotrichum kahawae </em>sp. nov.. <em>Mycological Research</em> 97 (8): 989–994.&nbsp;</p>
<p>Wang, Q.H., Fan, K., Li, D.W., Han, C.M., Qu, Y.Y. &amp; Wu, X.Q. (2019) Identification, Virulence and Fungicide Sensitivity of <em>Colletotrichum gloeosporioides</em> s.s. Responsible for Walnut Anthracnose Disease in China. <em>Plant Disease</em> 104 (5): 1358–1368.&nbsp;</p>
<p>Wang, Q.H., Fan, K., Li, D.W., Niu, S.G., Hou, L.Q. &amp; Wu X.Q. (2017) Walnut anthracnose caused by <em>Colletotrichum siamense</em> in China. <em>Australasian</em> <em>Plant Pathology</em> 46: 585–595.&nbsp;</p>
<p>Wang, Q.H., Li, D.W., Duan, C.H., Liu, X.H., Niu, S.G., Hou, L.Q. &amp; Wu, X.Q. (2018) First report of walnut anthracnose caused by <em>Colletotrichum fructicola</em> in China. <em>Plant Disease</em> 102 (1): 247.&nbsp;</p>
<p>Wang, Q.H., Liu, X.H., Fan, K., Duan, C.H., Niu, S.G. &amp; Wu, X.Q. (2016) Identification and biological characteristics of pathogen from <em>Colletotrichum gloeosporioides</em>. <em>Journal of Shandong Agricultural University (Natural Science)</em> 47: 9–14.</p>
<p>Wang, Q.Q., Tang, G.H. (2018) The mitochondrial genomes of two walnut pests, <em>Gastrolina depressa</em> <em>depressa</em> and <em>G. depressa thoracica</em> (Coleoptera: Chrysomelidae), and phylogenetic analyses. <em>PeerJ</em> 6: e4919.&nbsp;</p>
<p>Wang, X., Liu, X., Wang, R., Lei, F.A. &amp; Hou, X. (2020) First report of <em>Colletotrichum aenigma</em> causing walnut anthracnose in China. <em>Plant disease</em> 105: 225.&nbsp;</p>
<p>Watanabe, M., Lee, K., Goto, K., Kumagai, S., Sugita-Konishi, Y., Hara-Kudo, Y. (2010) Rapid and effective DNA extraction method with bead grinding for a large amount of fungal DNA. <em>Journal of Food Protection</em> 73 (6): 1077–1084.&nbsp;</p>
<p>Weir, B.S., Johnston, P.R. &amp; Damm, U. (2012) The <em>Colletotrichum gloeosporioides </em>species complex. <em>Studies in Mycology</em> 73: 115–180.&nbsp;</p>
<p>White, T.J., Bruns, T., Lee, S. &amp; Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. <em>In:</em> Innis, M.A., Gelfand, D.H., Sninsky, J.J. &amp; White, T.J. (Eds) <em>PCR protocols, a guide to methods and applications.</em> Academic Press, California, pp. 315–322.</p>
<p>Yang, Y.L., Liu, Z.Y., Cai, L., Hyde, K.D., Yu, Z.N. &amp; McKenzie, E.H.C. (2009) <em>Colletotrichum</em> anthracnose of Amaryllidaceae. <em>Fungal Diversity</em> 39: 123–146.&nbsp;</p>
<p>Zhu, Y., Liao, W., Zou, D., Wu, Y. &amp; Zhou, Y. (2015) First report of leaf spot disease on walnut caused by <em>Colletotrichum fioriniae</em> in China. <em>Plant Disease</em> 99: 289.</p>
<p>Zhu, Y.F., Yin, Y.F., Qu, W.W. &amp; Yang, K. (2014) Morphological and molecular identification of <em>Colletotrichum gloeosporioides</em> causing walnut anthracnose in Shandong province, China. <em>Acta Horticulturae</em> 1050: 353–359.&nbsp;</p>