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Phylogenetic relationship and fungicide sensitivity of members of the Colletotrichum gloeosporioides species complex from apple

  • Fungal Diseases
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Abstract

The members of the Colletotrichum gloeosporioides species complex (CGSC), the dominant pathogens of apple bitter rot in Nagano prefecture, Japan, were reidentified and the relationship between the species and fungicide sensitivity was revealed. Based on phylogenetic analysis of the ApMat locus with the neighbor-joining (NJ) method, isolates from apple contained three species of the CGSC; C. fructicola, C. aenigma, C. siamense, and three clades of the CGSC: Clade V, S and K. Colletotrichum fructicola and Clade S dominated in Nagano Prefecture. Isolates of C. siamense, C. aenigma and Clade V, S and K remained sensitive to benomyl and quinone outside inhibitor (QoI) fungicides, while C. fructicola often developed resistance to benomyl and QoI fungicides. These results suggest that the development of fungicide resistance differs among members of the CGSC.

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References

  • Akahira T, Hanaoka T (2013) Occurrence of trifloxystrobin resistant strains of Colletotrichum gloeosporioides (Glomerella cingulata), the causal fungus of apple bitter rot in Aomori Prefecture. Jpn J Phytopathol 79:197–198 ​(Abstract in Japanese)

    Google Scholar 

  • Alaniz S, Hernández L, Mondino P (2015) Colletotrichum fructicola is the dominant and one of the most aggressive species causing bitter rot of apple in Uruguay. Trop Plant Pathol 40:265–274

    Article  Google Scholar 

  • Baroncelli R, Sreenivasaprasad S, Thon MR, Sukno SA (2014) First report of apple bitter rot caused by Colletotrichum godetiae in the United Kingdom. Plant Dis 98:1000

    Article  Google Scholar 

  • Braganca CAD, Damm U, Baroncelli R, Massola Jr NS, Crous PW (2016) Species of the Colletotrichum acutatum complex associated with anthracnose diseases of fruit in Brazil. Fungal Biol 120:547–561

    Article  PubMed  Google Scholar 

  • Chethana CS, Chowdappa P, Biju CN, Praveena R, Sujatha AM (2016) Molecular and phenotypic characterization revealed six Colletotrichum species responsible for anthracnose disease of small cardamom in South India. Eur J Plant Pathol 146:465–481

    Article  CAS  Google Scholar 

  • Chung W, Ishii H, Nishimura K, Fukaya M, Yano K, Kajitani Y (2006) Fungicide sensitivity and phylogenetic relationship of anthracnose fungi isolated from various fruit crops in Japan. Plant Dis 90:506–512

    Article  CAS  Google Scholar 

  • Damm U, Cannon PF, Woudenberg JHC, Crous PW (2012) The Colletotrichum acutatum species complex. Stud Mycol 73:37–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evol Int J org Evol 39:783–791

    Article  Google Scholar 

  • Fungicide Resistance Action Committee (2014) Pathogen risk list 2014. Fungicide Resistance Action Committee, CropLife International, Brussells, Belgium. http://www.frac.info/docs/default-source/publications/pathogen-risk/pathogen-risk-list.pdf. Accessed 30 Apr 2017

  • Gan P, Nakata N, Suzuki T, Shirasu K (2017) Markers to differentiate species of anthracnose fungi identify Colletotrichum fructicola as the predominant virulent species in strawberry plants in Chiba Prefecture of Japan. J Gen Plant Pathol 83:14–22

    Article  CAS  Google Scholar 

  • Gisi U, Sierotzki H, Cook A, McCaffery A (2002) Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Manag Sci 58:859–867

    Article  CAS  PubMed  Google Scholar 

  • Hirayama Y, Asano S, Watanabe K, Sakamoto Y, Ozaki M, Okayama K, Ohki ST, Tojo M (2016) Control of Colletotrichum fructicola on strawberry with a foliar spray of neutral electrolyzed water through an overhead irrigation system. J Gen Plant Pathol 82:186–189

    Article  CAS  Google Scholar 

  • Inada M, Ishii H, Chung W, Yamada T, Yamaguchi J, Furuta A (2008) Occurrence of strobilurin resistant strains of Colletotrichum gloeosporioides (Glomerella cingulata), the causal fungus of strawberry anthracnose. Jpn J Phytopathol 74:114–117 (Japanese with English summary)

    Article  CAS  Google Scholar 

  • Ishii H (2009) Corynespora cassiicola. In: Manual of sensitivity to fungicide of plant pathogens II. Japan Plant Protection Association, Tokyo, pp 69–71

    Google Scholar 

  • Ishii H, Fraaije BA, Sugiyama T, Noguchi K, Nishimura K, Takeda T, Amano T, Hollomon DW (2001). Occurrence and molecular characterization of strobilurin resistance in cucumber powdery mildew and downy mildew. Phytopathology 91:1166–1171

    Article  CAS  PubMed  Google Scholar 

  • Ishii H, Fountaine J, Chung WH, Kansako M, Nishimura K, Takahashi K, Oshima M (2009) Characterisation of QoI-resistant field isolates of Botrytis cinerea from citrus and strawberry. Pest Manag Sci 65:916–922

    Article  CAS  PubMed  Google Scholar 

  • Jayawardena RS, Hyde KD, Damm U, Cai L, Liu M, Li XH, Zhang W, Zhao WS, Yan JY (2016) Notes on currently accepted species of Colletotrichum. Mycosphere 7:1192–1260

    Google Scholar 

  • Kawai Y, Kondo K, Okazawa K, Miyazawa T (2000) Distribution of apple bitter rot caused by Colletotrichum acutatum in Nagano Prefecture (in Japanese). Annual Report of the Kanto-Tosan Plant Protection. Society 47:79–81

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kuck KH (2007) QoI fungicides: resistance mechanisms and its practical importance. In: Ohkawa H, Miyagawa H, Lee PW (eds) Pesticide chemistry; Crop protection, public health, environmental safety. Wiley-VCH, Weinheim, pp 275–283

    Google Scholar 

  • Liu F, Weir B S, Damm U, Crous P W, Wang Y, Liu B, Wang M, Zhang M, Cai L (2015) Unravelling Colletotrichum species associated with Camellia: employing ApMat and GS loci to resolve species in the C. gloeosporioides complex. Persoonia 35:63–86

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu F, Wang M, Damm U, Crous PW, Cai L (2016) Species boundaries in plant pathogenic fungi: a Colletotrichum case study. BMC Evol Biol 16:81

    Article  PubMed  PubMed Central  Google Scholar 

  • Munir M, Amsden B, Dixon E, Vaillancourt L, Ward Gauthier NA (2016) Characterization of Colletotrichum species causing bitter rot of apple in Kentucky orchards. Plant Dis 100:2194–2203

    Article  Google Scholar 

  • Peres NAR, Souza NL, Peever TL, Timmer LW (2004) Benomyl sensitivity of isolates of Colletotrichum acutatum and C. gloeosporioides from citrus. Plant Dis 88:125–130

    Article  CAS  Google Scholar 

  • Prihastuti H, Cai L, Chen H, McKenzie EHC, Hyde KD (2009) Characterization of Colletotrichum species associated with coffee berries in northern Thailand. Fungal Divers 39:89–109

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sato T (1997) Characters and identification of a plurivorus anthracnose fungus, Colletotrichum acutatum (in Japanese with English summary). Proc Assoc Pl Protec Shikoku 32:1–19

    Google Scholar 

  • Sato T, Moriwaki J (2013) Molecular re-identification of strains in NIAS Genebank belonging to phylogenetic groups A2 and A4 of the Colletotrichum acutatum species complex. Microbiol Cult Coll 29:13–23

    Google Scholar 

  • Sato T, Uematsu S, Iijima Y, Koganezawa H (1998) Occurrence of apple bitter rot by grayish colony form of Colletotrichum acutatum in Japan and pathogenicity to apple fruits of C. acutatum and Glomerella cingulata isolated from other plants (in Japanese with English summary). Trans Mycol Soc Jpn 39:35–44

    Google Scholar 

  • Sato T, Moriwaki J, Misawa T (2013) Molecular re-identification of strains of the Colletotrichum acutatum species complex deposited in the NIAS Genebank and morphological characteristics of its member species. JARQ 47:295–305

    Article  Google Scholar 

  • Sato T, Aoki T, Nemoto H (2016) Molecular re-identification of MAFF (NIAS Genebank) strains belonging to the Colletotrichum gloeosporioides species complex (abstract in Japanese). Microb Resour Syst 32:77–78

    Google Scholar 

  • Sato T, Moriwaki J, Aoki T, Nemoto H (2017) Update of pathogen names of several anthracnose based on molecular re-identification of NIAS Genebank strains belonging to the Colletotrichum gloeosporioides species complex (abstract in Japanese). Jpn J Phytopathol 83:43–44

    Google Scholar 

  • Sharma G, Kumar N, Weir BS, Hyde K, Shenoy BS (2013) The ApMat marker can resolve Colletotrichum species: a case study with Mangifera indica. Fungal Divers 61:117–138

    Article  Google Scholar 

  • Sharma G, Pinnaka AK, Shenoy BD (2015) Resolving the Colletotrichum siamense species complex using ApMat marker. Fungal Divers 71:247–264

    Article  Google Scholar 

  • Silva D, Várzea P, Cai L, Paulo O, Batista D (2012) Application of the Apn2/MAT locus to improve the systematics of the Colletotrichum gloeosporioides complex: an example from coffee (Coffea spp.) hosts. Mycologia 104:396–409

    Article  CAS  PubMed  Google Scholar 

  • Tamura T, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson J, Higgins D, Gibson T (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velho A, Alaniz S, Casanova L, Mondino P, Stadnik M (2015) New insights into the characterization of Colletotrichum species associated with apple diseases in southern Brazil and Uruguay. Fungal Biol 119:229–244

    Article  PubMed  Google Scholar 

  • Wang W, Fu D, Zhang R, Sun G (2015) Etiology of apple leaf spot caused by Colletotrichum spp. (in Chinese with English summary). Mycosystema 34:13–25

    Google Scholar 

  • Weir BS, Johnston PR, Damm U (2012) The Colletotrichum gloeosporioides species complex. Stud Mycol 73:115–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wenneker K, Pham KTK, Lemmers MEC, de Boer FA, van der Lans AM, van Leeuwen PJ, Hollinger TC (2016) First report of Colletotrichum godetiae causing bitter rot on ‘Golden Delicious’ apples in the Netherlands. Plant Dis 100:218

    Article  Google Scholar 

  • Yokosawa S, Sato T, Kondo K (2015) Identification of the Colletotrichum gloeosporioides species complex members isolated from apple and grape in Nagano (abstract in Japanese). Jpn J Phytopathol 81:206

    Google Scholar 

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Acknowledgements

We thank Mr. Yasuhiko Iwanami and the Nagano Prefecture Agricultural Extension Center for help in material collections; Mr. Kazuya Minemura, Ms. Akiko Yokota and Ms. Mariko Katsuyama for technical assistance; and Mr. Shuichi Kato for helpful suggestions in this study.

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Author notes

  1. Ken-ichi Kondo

    Present address: Nagano Prefecture Agricultural Experiment & Extension Division, Nagano, Nagano, 380–8570, Japan

Authors and Affiliations

  1. Nagano Prefecture Fruit Tree Experimental Station, Suzaka, Nagano, 382-0072, Japan

    Shiori Yokosawa, Naoki Eguchi & Ken-ichi Kondo

  2. Genetic Resources Center, National Agriculture and Food Research Organization, Tsukuba, Ibaraki, 305-8602, Japan

    Toyozo Sato

Authors
  1. Shiori Yokosawa
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  2. Naoki Eguchi
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  3. Ken-ichi Kondo
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  4. Toyozo Sato
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Correspondence to Shiori Yokosawa.

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Yokosawa, S., Eguchi, N., Kondo, Ki. et al. Phylogenetic relationship and fungicide sensitivity of members of the Colletotrichum gloeosporioides species complex from apple. J Gen Plant Pathol 83, 291–298 (2017). https://doi.org/10.1007/s10327-017-0732-9

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  • DOI: https://doi.org/10.1007/s10327-017-0732-9

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