Abstract
The species composition of the strawberry anthracnose pathogen population in Saga Prefecture was investigated through phylogenetic analysis of the nucleotide sequences of the intergenic regions of the apn2 and MAT1-2–1 genes. Here, 77 out of the 80 Colletotrichum isolates used were classified as C. fructicola, and the remaining three were classified as C. siamense. The 77 C. fructicola isolates were tested for sensitivity to fludioxonil, which is widely used as the main fungicide in rotational programs in Saga Prefecture. High levels of resistance to fludioxonil were observed in 14 C. fructicola isolates tested for sensitivity to mycelial growth in fludioxonil-containing media. Furthermore, two inoculation assays using strawberry seedlings treated with fludioxonil were performed on five of the 14 isolates that showed high levels of resistance. The effectiveness of fludioxonil was significantly low in these isolates. To our knowledge, this is the first study to report fludioxonil resistance in a C. fructicola population.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adachi M, Watanabe H (2014) The current situation of fungal pathogen resistant to fungicides for the strawberry anthracnose and control effect of fungicides in Gifu prefecture (in Japanese). Ann Rept Kansai Pl Prot 56:80–90
Dowling M, Peres N, Villani S, Schnabel G (2020) Managing Colletotrichum on fruit crops; a ‘complex’ challenge. Plant Dis 104:2301–2316
Egashira M, Teramoto T, Nakamura Y, Mori M (2016) Species composition and fungicide susceptibility of strawberry anthracnose in Nagasaki Prefecture (in Japanese). Nagasaki Research Results Information. Available via DIALOG. https://www.pref.nagasaki.jp/e-nourin/nougi/theme/result/H28seika-jouhou/shidou/S-28-19.pdf. Cited 5 Jan 2023
Hirayama Y, Kawamoto Y, Matsutani S, Nishizaki M, Okayama K (2008) Occurrence of fungicides resistant isolates of Glomerella cingulata causing the strawberry anthracnose in Nara Prefecture (in Japanese). Ann Rept Kansai Pl Prot 50:93–94
Hirayama Y, Nishizaki M, Okayama K (2010) Control of strawberry anthracnose caused by Glomerella cingulata using systematic application of fungicides (in Japanese with English summary). Bull Nara Agr Exp Sta 41:17–21
Ibaraki Agricultural Center (2020) Species composition and fungicide susceptibility of strawberry anthracnose in Ibaraki Prefecture (in Japanese). Horticultural Research Institute Research Results. Available via DIALOG. https://www.pref.ibaraki.jp/nourinsuisan/enken/seika/yasai/ichigo/documents//r2yasai3.pdf. Cited 5 Jan 2023
Inada M, Furuta A (2011) Dispersal of strawberry anthracnose in symptomless plants infected with Glomerella cingulata by rainfall and irrigation (in Japanese). Kyushu Pl Prot Res 57:45–50
Inada M, Yamaguchi J, Furuta A (2005) Control of strawberry anthracnose (Glomerella cingulata) by rain shelter and systematic application of fungicides (in Japanese with English summary). Kyushu Pl Prot Res 51:15–20
Inada M, Ishii H, Chung WH, Yamada T, Yamaguchi J, Furuta A (2008) Occurrence of strobilurin resistant strains of Colletotrichum gloeosporioides (Glomerella cingulata), the causal fungus of strawberry anthracnose (in Japanese with English summary). Jpn J Phytopathol 74:114–117
Inada M, Yamaguchi J, Furuta A (2009) Occurrence of benzimidazole- and diethofencarb-resistant strains of Glomerella cingulata, the causal fungus of strawberry anthracnose in Saga prefecture and the effects of several fungicides (in Japanese with english summary). Kyushu Pl Prot Res 55:31–36
Inada M, Yamaguchi J, Furuta A (2010) An agar dilution method to test the sensitivity of Glomerella cingulata, causal fungus of strawberry anthracnose, to azoxystrobin (in Japanese with english summary). Jpn J Phytopathol 76:1–6
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
Kanda Y (2013) Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 48:452–458
Kikuchi M, Ogawara T, Hashimoto Y, Miyamoto T, Kaneda M, Tomita Y (2010) Identification of Colletotrichum species causing strawberry anthracnose and distribution of fungal strains resistant to some fungicides in Ibaraki prefecture (in Japanese with English summary). Bull Hortic Inst Ibaraki Agric Center 17:35–42
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
Kuang J, Hou YP, Wang JX, Zhou MG (2011) Sensitivity of Sclerotinia sclerotiorum to fludioxonil: In vitro determination of baseline sensitivity and resistance risk. Crop Prot 30:876–882
Liu F, Weir BS, Damm U, Crous PW, 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
MacKenzie SJ, Peres NA (2012) Use of leaf wetness and temperature to time fungicide applications to control anthracnose fruit rot of strawberry in Florida. Plant Dis 96:522–528
Nakano T (2020) Fungicides acting on signal transduction (in Japanese). Plant Prot 74:315–318
Prihastuti H, Cai L, Chen H, McKenzie EHC, Hyde KD (2009) Characterization of Colletotrichum species associated with coffee berries in northern Thailand. Fungal Diversity 39:89–109
Sato T and Moriwaki J (2003) Plurivorous plant anthracnose fungus, Colletotrichum acutatum (in Japanese). In MAFF Microorganism Genetic Resources Manual No.13. National Institute of Agrobiological Sciences, Japan. Available via DIALOG. https://www.gene.affrc.go.jp/pdf/manual/micro-13.pdf. Cited 14 Feb 2024
Schnabel G, Tan Q, Schneider V, Ishii H (2021) Inherent tolerance of Colletotrichum gloeosporioides to fludioxonil. Pestic Biochem Physiol 172:104767
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
Sharma G, Pinnaka AK, Shenoy BD (2015) Resolving the Colletotrichum siamense species complex using ApMat marker. Fungal Divers 71:247–264
Shirasu K (2018) Comparative genomics-based analysis of strawberry anthracnose pathogens (in Japanese). Plant Prot 72:232–235
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
Takeyama K, Ishii N, Uchida Y, Matsusaki M (2022) Chemical control system for strawberry anthracnose during the nursery period (in Japanese with English summary). Ann Rept Kansai Pl Prot 64:105–107
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027
Yokosawa S, Eguchi N, Kondo K, Sato T (2017) Phylogenetic relationship and fungicide sensitivity of members of the Colletotrichum gloeosporioides species complex from apple. J Gen Plant Pathol 83:291–298
Yonezawa A (2010) Occurrence of azoxystrobin-resistant strains of Glomerella cingulata causing strawberry anthracnose in Kagawa prefecture and the effects of several fungicides (in Japanese with English summary). Bull Kagawa Pref Agric Exp Stn 61:21–27
Zhou F, Hu HY, Song YL, Gao YQ, Liu QL, Song PW, Chen EY, Yu YA, Li DX, Li CW (2020) Biological characteristics and molecular mechanism of fludioxonil resistance in Botrytis cinerea from henan province of China. Plant Dis 104:1041–1047
Acknowledgements
We would like to thank Editage (www.editage.jp) for English language editing.
Author information
Authors and Affiliations
Contributions
AF and YI designed the study and the main conceptual ideas. MK developed the statistical analysis plan and conducted sequencing and phylogenic analyses. NT contributed to the interpretation of the results. AF wrote the original manuscript with support from YI and MK. YI and MK supervised this study. All authors reviewed the manuscript draft and revised it critically on intellectual content. All authors approved the final version of the manuscript to be published.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
10327_2024_1174_MOESM1_ESM.xlsx
Supplementary file1 Species identification of the Colletotrichum field isolates used in this study The effect of fludioxonil on the mycelial growth of Colletotrichum isolates collected from strawberries in Saga Prefecture (XLSX 24 KB) Supplementary file2 (XLSX 24 KB)
10327_2024_1174_MOESM4_ESM.pptx
Supplementary file4 The taxonomic status of Colletotrichum isolates from strawberry in Saga Prefecture, as inferred from phylogenetic analysis based on sequences of the intergenic region of apn2 and MAT1-2–1 (ApMat) (PPTX 53 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Furuta, A., Ide, Y., Tashiro, N. et al. First report of fludioxonil resistance isolate of Colletotrichum fructicola emerging on strawberry in Japan. J Gen Plant Pathol (2024). https://doi.org/10.1007/s10327-024-01174-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10327-024-01174-4