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Article
Published: 2022-08-08

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

Abstract

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.

References

  1. Abate, D., Pastore, C., Gerin, D., De Miccolis Angelini, R.M., Rotolo, C., Pollastro, S. & Faretra, F. (2018) Characterization of Monilinia spp. populations on stone fruit in South Italy. Plant Disease 102: 1708–1717.  https://doi.org/10.1094/PDIS-08-17-1314-RE

  2. Abbasi, K., Abbasi, S., Fotouhifar, K.B., Zebarjadi, A.R. & Cheghamirza, K. (2013) Genetic diversity of Cytospora chrysosperma isolates obtained from Iranian walnut trees using molecular markers. African Journal of Biotechnology 10: 15710–15716.  https://doi.org/10.5897/AJB11.1225

  3. An, H. & Yang, K. (2014) Resistance gene analogs in walnut (Juglans regia) conferring resistance to Colletotrichum gloeosporioides. Euphytica 197: 175–190.  https://doi.org/10.1007/s10681-013-1050-8

  4. Arx, J.A.V. (1957) Die arten der gattung Colletotrichum Cda. Phytopathologische Zeitschrift 29: 413–468.

  5. 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. & Johnston, P.R. (2009) A polyphasic approach for studying Colletotrichum. Fungal Diversity 39: 183–204.  https://doi.org/10.1016/j.riam.2009.11.001

  6. Cannon, P.F., Buddie, A.G. & Bridge, P.D. (2008) The typification of Colletotrichum gloeosporioides. Mycotaxon 104: 189–204.

  7. Cannon, P.F., Damm, U., Johnston, P.R. & Weir, B.S. (2012) Colletotrichum–current status and future directions. Studies in Mycology 73: 181–213.  https://doi.org/10.3114/SIM0014

  8. Carbone, I. & Kohn, L.M. (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553–556.  https://doi.org/10.1080/00275514.1999.12061051

  9. Corda, A.C.I. (1831) Die Pilze Deutschlands. In: Sturm, J. (Ed.) Deutschlands Flora in Abbildungen nach der Natur mit Beschreibungen. Sturm, Nürnberg 3 (12): 33–64.

  10. Crouch, J.A. (2014) Colletotrichum caudatum s. l. is a species complex. IMA Fungus 5: 17–30.  https://doi.org/10.5598/imafungus.2014.05.01.03

  11. Crouch, J.A., Clarke, B.B. & Hillman, B.I. (2009) What is the value of ITS sequence data in Colletotrichum systematics and species diagnosis? A case study using the falcate–spored graminicolous Colletotrichum group. Mycologia 101: 648–656.  https://doi.org/10.3852/08-231

  12. Damm, U., Cannon, P.F., Woudenberg, J.H.C. & Crous, P. (2012a) The Colletotrichum acutatum species complex. Studies in Mycology 73: 37–113.  https://doi.org/10.3114/sim0010

  13. Damm, U., Cannon, P.F., Woudenberg, J.H.C., Johnston, P.R., Weir, B.S., Tan, Y.P., Shivas, R.G. & Crous, P.W. (2012b) The Colletotrichum boninense species complex. Studies in Mycology 73: 1–36.  https://doi.org/10.3114/sim0002

  14. Damm, U., Sato, T., Alizadeh, A., Groenewald, J.Z. & Crous, P.W. (2019) The Colletotrichum dracaenophilum, C. magnum and C. orchidearum species complexes. Studies in Mycology 92: 1–46.  https://doi.org/10.1016/j.simyco.2018.04.001

  15. Damm, U., Woudenberg, J.H.C., Cannon, P.F. & Crous, P.W. (2009) Colletotrichum species with curved conidia from herbaceous hosts. Fungal Diversity 39: 45–87.  https://doi.org/10.1016/j.riam.2009.11.001

  16. 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. & Foster, G.D. (2012) The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13: 414–430.  https://doi.org/10.1111/ J.1364-3703.2011.00783.X

  17. Doyle, V.P., Oudemans, P.V., Rehner, S.A. & Litt, A. (2013) Habitat and host indicate lineage identity in Colletotrichum gloeosporioides s. l. from wild and agricultural landscapes in North America. PLoS ONE 8 (5): e62394. https://doi.org/10.1371/journal.pone.0062394

  18. Guerber, J.C., Liu, B., Correll, J.C. & Johnston, P.R. (2003) Characterization of diversity in Colletotrichum acutatum sensu lato by sequence analysis of two gene introns, mtDNA and intron RFLPs, and mating compatibility. Mycologia 95: 872–895. https://doi.org/10.1080/15572536.2004.11833047

  19. Hall, T.A. (1999) Bioedit: a user–friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98. https://doi.org/10.1021/bk-1999-0734.ch008

  20. He, L., Li, X., Gao, Y., Li, B., Mu, W. & Liu, F. (2019) Characterization and fungicide sensitivity of Colletotrichum spp. from different hosts in Shandong, China. Plant Disease 103 (1): 34–43.  https://doi.org/10.1094/PDIS-04-18-0597-RE

  21. Jayawardena, R.S., Hyde, K.D., Damm, U., Cai, L., Liu, M., Li, X.H., Zhang, W., Zhao, W.S. & Yang, J.Y. (2016) Notes on currently accepted species of Colletotrichum. Mycosphere 7 (8): 1192–1260.  https://doi.org/10.5943/mycosphere/si/2c/9

  22. Khan, A.A. & Kundoo, A.A. (2018) Pests of walnut. In: Pests and Their Management. pp. 605–647.  https://doi.org/10.1007/978-981-10-8687-8_19

  23. Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Molecular Biology and Evolution 33 (7): 1870–1874.  https://doi.org/10.1093/MOLBEV/MSW054

  24. Lio, D.D., Cobo–Díaz, J.F., Masson, C., Chalopin, M., Kebe, D., Giraud, M., Verhaeghe, A., Nodet, P., Sarrocco, S. & Floch, G.L. (2018) Combined metabarcoding and multi–locus approach for genetic characterization of Colletotrichum species associated with common walnut (Juglans regia) anthracnose in France. Scientific Reports 8: 10765.  https://doi.org/10.1038/s41598-018-29027-z

  25. Liu, F., Cai, L., Crous, P.W. & Damm, U. (2014) The Colletotrichum gigasporum species complex. Persoonia 33: 83–97.  https://doi.org/10.3767/003158514X684447

  26. Liu, F., Wang, M., Damm, U., Crous, P.W. & Cai, L. (2016) Species boundaries in plant pathogenic fungi: a Colletotrichum case study. BMC Evolutionary Biology 16: 81.  https://doi.org/10.1186/s12862-016-0649-5

  27. Liu, X.Y., Yao, J. & Yang, J.X. (1995) A study on Colletotrichum classification of wooden plant in Shaanxi province. Journal of Northwest Forestry College 3: 29–30.

  28. 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. & Crous, P.W. (2017) Genera of phytopathogenic fungi: GOPHY 1. Studies in Mycology 86: 99–216.  https://doi.org/10.1016/j.simyco.2017.04.002

  29. Mills, P.R., Hodson, A., Brown, A.E. (1992) Molecular differentiation of Colletotrichum gloeosporioides isolates infecting tropical fruits. In: Bailey, J.A. & Jeger, M.J. (eds.) Colletotrichum: Biology, Pathology and Control. CABI, Wallingford, UK, pp. 269–288.

  30. Mu, T., Zhang, Z., Liu, R., Liu, S., Li, Z., Zhang, X. & Xia, J. (2021) Morphological and molecular phylogenetic analyses reveal three species of Colletotrichum in Shandong province, China. MycoKeys 85: 57–71.  https://doi.org/10.3897/mycokeys.85.75944

  31. Munir, M., Amsden, B., Dixon, E., Vaillancourt, L. & Gauthier, N.A.W. (2016) Characterization of Colletotrichum species causing bitter rot of apple in Kentucky orchards. Plant Disease 100 (11): 2194–2203.  https://doi.org/10.1094/PDIS-10-15-1144-RE

  32. Nirenberg, H.I. (1976) Untersuchungen uber die morphologische und biologische differenzierung in der fusaium-sektion liseola. Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft, Berlin-Dahlem 169: 1–117.

  33. Qu, W.W., Yang, K.Q., Liu, H.X. & Hou, L.Q. (2011) Main diseases of walnut and integrated management in Shandong. Plant Protection 44: 136–140.  https://doi.org/10.3969/j.issn.0529-1542.2011.02.030

  34. 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 Teratosphaeriaceae. Persoonia 33: 1–40.  https://doi.org/10.3767/003158514X681981

  35. Rambaut, A., Drummond, A. (2010) FigTree v.1.3.1. Institute of evolutionary biology, University of Edinburgh, Edinburgh, UK.

  36. Ronquist, F., Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.  https://doi.org/10.1093/BIOINFORMATICS/BTG180

  37. Samarakoon, M.C., Peršoh, D., Hyde, K.D., Bulgakov, T.S., Manawasinghe, I.S., Jayawardena, R.S., Promputtha, I. (2018) Colletotrichum acidae sp. nov. from northern Thailand and a new record of C. dematium on Iris sp.. Mycosphere 9 (3): 583–597.  https://doi.org/10.5943/mycosphere/9/3/9

  38. Sharma, G., Kumar, N., Weir, B.S., Hyde, K.D. & Shenoy, B.D. (2013) The ApMat marker can resolve Colletotrichum species: a case study with Mangifera indica. Fungal Diversity 61: 117–138.  https://doi.org/10.1007/s13225-013-0247-4

  39. Squissato, V., Yucel, Y.H., Richardson, S.E., Alkhotani, A., Wong, D.T., Nijhawan, N. & Chan, C.C. (2015) Colletotrichum truncatum species complex: treatment considerations and review of the literature for an unusual pathogen causing fungal keratitis and endophthalmitis. Medical Mycology Case Reports 9: 1–6. https://doi.org/10.1016/j.mmcr.2015.06.001

  40. Sreenivasaprasad, S., Brown, A.E. & Mills, P.R. (1992) DNA sequence variation and interrelationship among Colletotrichum species causing strawberry anthracnose. Physiological and Molecular Plant Pathology 41: 265–281.  https://doi.org/10.1016/0885-5765(92)90026-R

  41. Stamatakis, A. (2014) RAxML Version 8: A tool for phylogenetic analysis and post–analysis of large phylogenies. Bioinformatics 30 (9): 1312–1313. https://doi.org/10.1093/bioinformatics/ btu033

  42. Sutton, B.C. (1980) The Coelomycetes. Fungi Imperfecti with Pycnidia, Acervuli and Stromata. Commonwealth Mycological Institute, Kew, 696 pp.

  43. Sutton, B.C. (1992) The genus Glomerella and its anamorph Colletotrichum. In: Colletotrichum: Biology, Pathology, and Control. CAB International, Wallingford, United Kingdom, 388 pp. [pp. 1–26.]

  44. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.  https://doi.org/10.1093/molbev/msr121

  45. Tan, X.D., Li, J.T., Bie, Z.R., Li, B.B. & Shu, H.W. (2020) Investigation and thinking on the development of Xingshan Walnut industry. Hubei Forestry Science and Technology 49 (04): 83–86. [CNKI: SUN: FBLI.0.2020-04-023]

  46. 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 Colletotrichum acutatum J.H. Simmonds. Fungal Diversity 28: 97–108.  https://doi.org/10.1002/yea.1554

  47. 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. MycoKeys 25–67.  https://doi.org/10.3897/mycokeys.33.23670

  48. Velho, A.C., Alaniz, S., Casanova, L., Mondino, P., Stadnik, M.J. & Schoch, C. (2015) New insights into the characterization of Colletotrichum species associated with apple diseases in southern Brazil and Uruguay. Fungal Biology 119: 229–244.  https://doi.org/10.1016/j.funbio.2014.12.009

  49. Vieira, W.A.S., Lima, W.G., Nascimento, E.S., Michereff, S.J., Câmara, M.P.S. & Doyle, V.P. (2017) The impact of phenotypic and molecular data on the inference of Colletotrichum diversity associated with Musa. Mycologia 109: 912–934.  https://doi.org/10.1080/00275514.2017.1418577

  50. Waller, J.M., Bridge, P.D., Black, R. & Hakiza, G. (1993) Characterization of the coffee berry disease pathogen, Colletotrichum kahawae sp. nov.. Mycological Research 97 (8): 989–994.  https://doi.org/10.1016/S0953-7562(09)80867-8

  51. Wang, Q.H., Fan, K., Li, D.W., Han, C.M., Qu, Y.Y. & Wu, X.Q. (2019) Identification, Virulence and Fungicide Sensitivity of Colletotrichum gloeosporioides s.s. Responsible for Walnut Anthracnose Disease in China. Plant Disease 104 (5): 1358–1368.  https://doi.org/10.1094/PDIS-12-19-2569-RE

  52. Wang, Q.H., Fan, K., Li, D.W., Niu, S.G., Hou, L.Q. & Wu X.Q. (2017) Walnut anthracnose caused by Colletotrichum siamense in China. Australasian Plant Pathology 46: 585–595.  https://doi.org/10.1007/s13313-017-0525-9

  53. Wang, Q.H., Li, D.W., Duan, C.H., Liu, X.H., Niu, S.G., Hou, L.Q. & Wu, X.Q. (2018) First report of walnut anthracnose caused by Colletotrichum fructicola in China. Plant Disease 102 (1): 247.  https://doi.org/10.1094/PDIS-06-17-0921-PDN

  54. Wang, Q.H., Liu, X.H., Fan, K., Duan, C.H., Niu, S.G. & Wu, X.Q. (2016) Identification and biological characteristics of pathogen from Colletotrichum gloeosporioides. Journal of Shandong Agricultural University (Natural Science) 47: 9–14.

  55. Wang, Q.Q., Tang, G.H. (2018) The mitochondrial genomes of two walnut pests, Gastrolina depressa depressa and G. depressa thoracica (Coleoptera: Chrysomelidae), and phylogenetic analyses. PeerJ 6: e4919.  https://doi.org/10.7717/peerj.4919

  56. Wang, X., Liu, X., Wang, R., Lei, F.A. & Hou, X. (2020) First report of Colletotrichum aenigma causing walnut anthracnose in China. Plant disease 105: 225.  https://doi.org/10.1094/PDIS-07-20-1430-PDN

  57. 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. Journal of Food Protection 73 (6): 1077–1084.  https://doi.org/10.1089/cmb.2008.0023

  58. Weir, B.S., Johnston, P.R. & Damm, U. (2012) The Colletotrichum gloeosporioides species complex. Studies in Mycology 73: 115–180.  https://doi.org/10.3114/sim0011

  59. White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds) PCR protocols, a guide to methods and applications. Academic Press, California, pp. 315–322.

  60. Yang, Y.L., Liu, Z.Y., Cai, L., Hyde, K.D., Yu, Z.N. & McKenzie, E.H.C. (2009) Colletotrichum anthracnose of Amaryllidaceae. Fungal Diversity 39: 123–146.  https://doi.org/10.1016/j.riam.2009.11.001

  61. Zhu, Y., Liao, W., Zou, D., Wu, Y. & Zhou, Y. (2015) First report of leaf spot disease on walnut caused by Colletotrichum fioriniae in China. Plant Disease 99: 289. https://doi.org/10.1094/PDIS-09-14-0938-PDN

  62. Zhu, Y.F., Yin, Y.F., Qu, W.W. & Yang, K. (2014) Morphological and molecular identification of Colletotrichum gloeosporioides causing walnut anthracnose in Shandong province, China. Acta Horticulturae 1050: 353–359.  https://doi.org/10.17660/ActaHortic.2014.1050.48