Published August 30, 2024 | Version v1
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Colletotrichum species (Glomerellales, Glomerellaceae) causing walnut anthracnose in China

  • 1. Beijing Forestry University, Beijing, China
  • 2. Qingdao Agricultural University, Shandong, China
  • 3. University of British Columbia, Vancouver, Canada

Description

Colletotrichum species can function as plant pathogens, saprobes or endophytes on a wide variety of plant hosts and are considered amongst the ten most significant genera of plant pathogens globally. China contributes almost half the walnut production in the world. However, Colletotrichum species occurring on walnut remain largely unresolved in China. To explore the Colletotrichum species found on walnut in China, 470 walnut fruit or leaf samples with anthracnose were collected from 14 main walnut-producing regions across seven provinces. A total of 165 Colletotrichum strains were isolated from these samples. The Colletotrichum isolates were identified, based on morphological characteristics and sequence analyses of ACT, CHS-1, GAPDH, ITS and TUB2. Twelve species, including 11 known Colletotrichum species (C. boninense, C. citrulli, C. fioriniae, C. fructicola, C. godetiae, C. juglandicola, C. karsti, C. mengyinense, C. pandanicola, C. peakense and C. siamense) and a novel species (C. chinensis sp. nov.) were identified. The species distribution revealed regional prevalence as follows: C. mengyinense was the most dominant species in Gansu, C. mengyinense and C. siamense in Shandong, C. chinensis in Beijing, C. pandanicola in Shaanxi and C. godetiae in Yunnan. Colletotrichum siamense was the sole species isolated in Sichuan and Xinjiang Provinces. Koch's postulates were fulfilled, demonstrating that all 12 species cause anthracnose on walnut. This is the first report of C. boninense, C. citrulli and C. karsti as pathogens of walnut anthracnose worldwide.

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References

  • Cannon PF, Buddie AG, Bridge PD (2008) The typification of Colletotrichum gloeosporioides. Mycotaxon 104: 189–204.
  • Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum - current status and future directions. Studies in Mycology 73: 181–213. https://doi.org/10.3114/sim0014
  • Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91(3): 553–556. https://doi.org/10.1080/00275514.1999.12061051
  • Chethana KWT, Manawasinghe IS, Hurdeal VG, Bhunjun CS, Appadoo MA, Gentekaki E, Raspé O, Promputtha I, Hyde KD (2021) What are fungal species and how to delineate them? Fungal Diversity 109(1): 1–25. https://doi.org/10.1007/s13225-021-00483-9
  • Cho SE, Oh JY, Lee DH, Kim CW (2023) First Report of Anthracnose on Juglans regia Caused by Colletotrichum siamense in Korea. Plant Disease 107(1): 218. https://doi.org/10.1094/PDIS-02-22-0267-PDN
  • Corda ACI (1831) In: Sturm J (Ed.) Deutschlands Flora in Abbildungen nach der Natur mit Beschreibungen. Sturm, Nürnberg 3(12), 33–64.
  • Da Lio D, Cobo-Díaz JF, Masson C, Chalopin M, Kebe D, Giraud M, Verhaeghe A, Nodet P, Sarrocco S, Le Floch G, Baroncelli R (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(1): 10765. https://doi.org/10.1038/s41598-018-29027-z
  • Damm U, Cannon PF, Woudenberg JHC, Crous PW (2012a) The Colletotrichum acutatum species complex. Studies in Mycology 73: 37–113. https://doi.org/10.3114/sim0010
  • Damm U, Cannon PF, Woudenberg JHC, Johnston PR, Weir BS, Tan YP, Shivas RG, Crous PW (2012b) The Colletotrichum boninense species complex. Studies in Mycology 73: 1–36. https://doi.org/10.3114/sim0002
  • Dowling M, Peres N, Villani S, Schnabel G (2020) Managing Colletotrichum on fruit crops: A "complex" challenge. Plant Disease 104(9): 2301–2316. https://doi.org/10.1094/PDIS-11-19-2378-FE
  • Fu M, Crous PW, Bai Q, Zhang PF, Xiang J, Guo YS, Zhao FF, Yang MM, Hong N, Xu WX, Wang GP (2019) Colletotrichum species associated with anthracnose of Pyrus spp. in China. Persoonia - Molecular Phylogeny and Evolution of Fungi 42: 1–35. https://doi.org/10.3767/persoonia.2019.42.01
  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Molecular Ecology 2(2): 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
  • Giraud M, Verhaeghe A (2015) Fiche bio-agresseur: Anthracnose à Colletotrichum sp. en verger de noyers. Arboric. Fruitière. 2.
  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61(4): 1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995
  • Guerber JC, Liu B, Correll JC, Johnston PR (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(5): 872–895. https://doi.org/10.1080/15572536.2004.11833047
  • Guo R (2016) Occurrence and control trend of main d es and pests of walnut in Baoji city. Northwest A&F University, China.
  • Guo Z, Luo CX, Wu HJ, Peng B, Kang BS, Liu LM, Zhang M, Gu QS (2022) Colletotrichum species associated with anthracnose disease of watermelon (Citrullus lanatus) in China. Journal of Fungi (Basel, Switzerland) 8(8): 790. https://doi.org/10.3390/jof8080790
  • He LF, Li XX, Gao YY, Li BX, 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
  • Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42(2): 182–192. https://doi.org/10.1093/sysbio/42.2.182
  • Iqra ul Haq I, Waseem Khan Qadri R, Amrao L, Ijaz S (2022) Effect of environmental conditions (temperature and precipitation) on severity of guava die-back caused by Colletotrichum spp. under climatic conditions of Pakistan. Journal of Plant Pathology 104: 1–12. https://doi.org/10.1007/s42161-021-00968-1
  • Jayawardena RS, Hyde KD, de Farias ARG, Bhunjun CS, Ferdinandez HS, Manamgoda DS, Udayanga D, Herath IS, Thambugala KM, Manawasinghe IS, Gajanayake AJ, Samarakoon BC, Bundhun D, Gomdola D, Huanraluek N, Sun YR, Tang X, Promputtha I, Thines M (2021) What is a species in fungal plant pathogens? Fungal Diversity 109(1): 239–266. https://doi.org/10.1007/s13225-021-00484-8
  • 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
  • Li FX, Chen JW, Chen Q, Liu ZY, Sun JY, Yan YT, Zhang HX, Bi Y (2023) Identification, pathogenicity, and sensitivity to fungicide of Colletotrichum species that causes walnut anthracnose in Beijing. Agronomy (Basel) 13(1): 214. https://doi.org/10.3390/agronomy13010214
  • Liu MZ, Li CH, Cao CM, Wang LQ, Li XP, Che J, Yang HM, Zhang XW, Zhao HY, He GZ, Liu XD (2021) Walnut fruit processing equipment: Academic insights and perspectives. Food Engineering Reviews 13(4): 1–36. https://doi.org/10.1007/s12393-020-09273-6
  • Liu F, Ma ZY, Hou LW, Diao YZ, Wu WP, Damm U, Song S, Cai L (2022) Updating species diversity of Colletotrichum, with a phylogenomic overview. Studies in Mycology 101(1): 1–56. https://doi.org/10.3114/sim.2022.101.01
  • Ma T, Yang C, Cai F, Chen Z (2022) Morpho-cultural, physiological and molecular characterisation of Colletotrichum nymphaeae causing anthracnose disease of walnut in China. Microbial Pathogenesis 166: 105537. https://doi.org/10.1016/j.micpath.2022.105537
  • Marin-Felix Y, Groenewald JZ, Cai L, Chen Q, Marincowitz S, Barnes I, Bensch K, Braun U, Camporesi E, Damm U, de Beer ZW, Dissanayake A, Edwards J, Giraldo A, Hernández-Restrepo M, Hyde KD, Jayawardena RS, Lombard L, Luangsa-ard J, McTaggart AR, Rossman AY, Sandoval-Denis M, Shen M, Shivas RG, Tan YP, van der Linde EJ, Wingfield MJ, Wood AR, Zhang JQ, Zhang Y, Crous PW (2017) Genera of phytopathogenic fungi: GOPHY 1. Studies in Mycology 86(1): 99–216. https://doi.org/10.1016/j.simyco.2017.04.002
  • Mu T, Zhang Z, Liu R, Liu S, Li Z, Zhang XG, Xia JW (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
  • O'Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within monophyletic lineage of the fungus Fusarium are nonorthologous. Molecular Phylogenetics and Evolution 7(1): 103–116. https://doi.org/10.1006/mpev.1996.0376
  • Pei D, Lu XZ (2011) Walnut germplasm resources in China. China Forestry Press, Beijing.
  • Réblová M, Miller AN, Rossman AY, Seifert KA, Crous PW, Hawksworth DL, Abdel-Wahab MA, Cannon PF, Daranagama DA, De Beer ZW, Huang SK, Hyde KD, Jayawardena R, Jaklitsch W, Gareth Jones EB, Ju YM, Judith C, Maharachchikumbura SSN, Pang KL, Petrini LE, Raja HA, Romero AI, Shearer C, Senanayake IC, Voglmayr H, Weir BS, Wijayawarden NN (2016) Recommendations for competing sexual-asexually typified generic names in Sordariomycetes (except Diaporthales, Hypocreales, and Magnaporthales). IMA Fungus 7(1): 131–153. https://doi.org/10.5598/imafungus.2016.07.01.08
  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029
  • Savian L, Muniz MFB, Poletto T, Maculan L, Rabuske JE, Blume E, Sarzi JS (2019) First report of Colletotrichum nymphaeae causing anthracnose on Juglans regia fruits in southern Brazil. Plant Disease 103(12): 3287. https://doi.org/10.1094/PDIS-06-19-1199-PDN
  • Stamatakis A (2014) RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30(9): 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
  • Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates Sunderland Massachusetts.
  • Talhinhas P, Baroncelli R (2021) Colletotrichum species and complexes: Geographic distribution, host range and conservation status. Fungal Diversity 110(1): 109–198. https://doi.org/10.1007/s13225-021-00491-9
  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30(12): 2725–2729. https://doi.org/10.1093/molbev/mst197
  • Varjas V, Kovács CS, Lakatos T, Tóth T, Bujdosó G (2019) First Report of Walnut Anthracnose Caused by Colletotrichum fioriniae on English (Persian) Walnut Fruits in Hungary. Plant Disease 103(11): 2964. https://doi.org/10.1094/PDIS-02-19-0286-PDN
  • Wang QH, Liu XH, Fan K, Duan CH, Niu SG, Wu XQ (2016) Identification and biological characteristics of pathogen from Colletotrichum gloeosporioides. Shandong Nongye Daxue Xuebao 47: 9–14.
  • Wang QH, Fan K, Li DW, Niu SG, Hou LQ, Wu XQ (2017) Walnut anthracnose caused by Colletotrichum siamense in China. Australasian Plant Pathology 46(6): 585–595. https://doi.org/10.1007/s13313-017-0525-9
  • Wang QH, Li DW, Duan CH, Liu XH, Niu SG, Hou LQ, Wu XQ (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
  • Wang XH, Liu X, Wang R, Fa L, Chen L, Xin XB, Zhang YG, Tian H, Xia MR, Hou X (2021) First report of Colletotrichum aenigma causing walnut anthracnose in China. Plant Disease 105(1): 225. https://doi.org/10.1094/PDIS-07-20-1430-PDN
  • Wang XH, Chen L, Ma QH, Liu X, Wang R, Fa L, Wang HX, Hou X, Xia MR, Yuan W (2023) First report of Colletotrichum godetiae causing anthracnose on walnut (Juglans regia and Juglans sigillata) in China. Plant Disease 107(8): 2544. https://doi.org/10.1094/PDIS-11-22-2625-PDN
  • Wei X, Yang SQ, Jiang ZG, Cui MJ, Deng JX, Zhang Y (2022) Colletotrichum juglandis sp. nov. (Ascomycota: Glomerellaceae) associated with walnut leaf spot in China. Phytotaxa 556(3): 256–268. https://doi.org/10.11646/phytotaxa.556.3.2
  • Weir BS, Johnston PR, Damm U (2012) The Colletotrichum gloeosporioides species complex. Studies in Mycology 73: 115–180. https://doi.org/10.3114/sim0011
  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (Eds) PCR Protocols: a Guide to Methods and Application. Academic Press, San Diego, CA, USA, 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  • Yu Z, Jiang X, Zheng H, Zhang H, Qiao M (2022) Fourteen new species of foliar Colletotrichum associated with the invasive plant Ageratina adenophora and surrounding crops. Journal of Fungi (Basel, Switzerland) 8(2): 185. https://doi.org/10.3390/jof8020185
  • Zhang L, Yin YQ, Zhao LL, Xie YQ, Han J, Zhang Y (2023) Two new species of Colletotrichum (Glomerellaceae, Glomerellales) causing walnut anthracnose in Beijing. MycoKeys 99: 131–152. https://doi.org/10.3897/mycokeys.99.106812
  • Zhu YF, Yin YF, Qu WW, Yang KQ (2014) Occurrence and spread of the pathogens on walnut (Juglans regia) in Shandong Province, China. Acta Horticulturae (1050): 347–351. https://doi.org/10.17660/ActaHortic.2014.1050.47
  • Zhu YZ, Liao WJ, Zou DX, Wu YJ, Zhou Y (2015) First report of leaf spot disease on walnut caused by Colletotrichum fioriniae in China. Plant Disease 99(2): 289. https://doi.org/10.1094/PDIS-09-14-0938-PDN