Abstract
Anthracnose is an important plant disease often caused by Colletotrichum spp. Fungicide resistance is a major challenge in controlling anthracnose. The Fungicide Resistance Action Committee (FRAC) reports that Colletotrichum species develop resistance against methyl benzimidazole carbamates (MBC), quinone-outside inhibitors (QoI), and demethylation inhibitors (DMI) fungicide classes. The high resistance of Colletotrichum species to MBC fungicides is attributed to the substitution of glutamic acid (E) with alanine (A) or lysine (K) in codon 198 of the nuclear β-tubulin (TUB2) gene (E198A/K mutation). Meanwhile, moderate MBC resistance is attributed to the substitution of phenylalanine (F) with tyrosine (Y) in codon 200 of TUB2 (F200Y mutation). High QoI-resistance is associated with the substitution of glycine (G) with alanine (A) in codon 143 of the mitochondrial cytochrome b (CYTB) gene (G143A mutation). On the other hand, moderate QoI resistance is attributed to the substitution of phenylalanine (F) with leucine (L) in codon 129 of CYTB (F129L mutation). In contrast to MBC- and QoI-resistance, which are associated with point mutations in the target genes, complex nucleotide mutations for DMI-resistance occur in the nuclear sterol 14α-demethylase (CYP51) gene. Taken together, these mutations in nucleotide/codon sequences cause changes in the translated amino acid residues, resulting in altered structure of proteins targeted by fungicides, thus affecting fungicide binding and effectivity. The underlying molecular mechanisms of fungicide resistance caused by these mutations, including the other resistance mechanisms independent from genetic mutations, are also reviewed. The distribution and phylogeography of reported Colletotrichum species that exhibit fungicide resistance are also discussed.
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References
Adaskaveg, J. E., & Hartin, R. J. (1997). Characterization of Colletotrichum acutatum isolates causing anthracnose of almond and peach in California. Phytopathology, 87(9), 979–987. https://doi.org/10.1094/PHYTO.1997.87.9.979
Ali, M. E., Hudson, O., Hemphill, W. H., Brenneman, T. B., & Oliver, J. E. (2019). First report of resistance to pyraclostrobin, boscalid, and thiophanate-methyl in Colletotrichum gloeosporioides from blueberry in Georgia. Plant Health Progress, 20(4), 261–262. https://doi.org/10.1094/PHP-08-19-0058-BR
Ali, M. E., Hudson, O., Waliullah, S., Cook, J., & Brannen, P. M. (2020). Sensitivity of Colletotrichum isolates collected from strawberries in Georgia to pyraclostrobin, a quinone outside inhibitor (QoI) fungicide. Plant Health Progress, 21(1), 69–70. https://doi.org/10.1094/PHP-12-19-0090-BR
Avila-Adame, C., Olaya, G., & Köller, W. (2003). Characterization of Colletotrichum graminicola isolates resistant to strobilurin-related QoI fungicides. Plant Disease, 87(12), 1426–1432. https://doi.org/10.1094/PDIS.2003.87.12.1426
Baggio, J. S., Wang, N. Y., Peres, N. A., & Amorim, L. (2018). Baseline sensitivity of Colletotrichum acutatum isolates from Brazilian strawberry fields to azoxystrobin, difenoconazole, and thiophanate-methyl. Tropical Plant Pathology, 43, 533–542. https://doi.org/10.1007/s40858-018-0232-2
Becher, R., & Wirsel, S. G. R. (2012). Fungal cytochrome P450 sterol 14α-demethylase (CYP51) and azole resistance in plant and human pathogens. Applied Microbiology and Biotechnology, 95, 825–840. https://doi.org/10.1007/s00253-012-4195-9
Bincader, S., Pongpisutta, R., & Rattanakreetakul, C. (2021). Colletotrichum species related to “Nam Dork Mai See Tong” mango in Central Thailand and risk detection of carbendazim-resistant strains. Research Square. Retrieved September 1, 2021, from https://doi.org/10.21203/rs.3.rs-782870/v1
Brent, K. J., & Hollomon, D. W. (1998). Fungicide resistance: the assessment of risk (Vol. 2). Brussels, Belgium: Global Crop Protection Federation.
Cai, M., Lin, D., Chen, L., Bi, Y., Xiao, L., & Liu, X. L. (2015). M233I mutation in the β-tubulin of Botrytis cinerea confers resistance to zoxamide. Scientific Reports, 5, 16881. https://doi.org/10.1038/srep16881
Chechi, A., Lewis Ivey, M. L., Kaufman, R. R., Bryson, K. P., & Schnabel, G. (2020). Quinone outside inhibitor-resistant Colletotrichum nymphaeae isolates from strawberry lack mutations in cytb gene. Journal of Plant Pathology, 102, 681–683. https://doi.org/10.1007/s42161-020-00565-8
Chechi, A., Stahlecker, J., Dowling, M. E., & Schnabel, G. (2019). Diversity in species composition and fungicide resistance profiles in Colletotrichum isolates from apples. Pesticide Biochemistry and Physiology, 158, 18–24. https://doi.org/10.1016/j.pestbp.2019.04.002
Chen S., Hu M., Schnabel G., Yang D., Yan X., Yuan H. (2020) Paralogous CYP51 genes of Colletotrichum spp. mediate differential sensitivity to sterol demethylation inhibitors. Phytopathology, 110(3), 615–625. https://doi.org/10.1094/PHYTO-10-19-0385-R
Chen, S., Schnabel, G., Yuan, H., & Luo, C. (2018a). LAMP detection of the genetic element ‘Mona’ associated with DMI resistance in Monilinia fructicola. Pest Management Science, 75(3), 779–786. https://doi.org/10.1002/ps.5178
Chen, S., Wang, Y., Schnabel, G., Peng, C. A., Lagishetty, S., Smith, K., Luo, C., & Yuan, H. (2018b). Inherent resistance to 14α-demethylation inhibitor fungicides in Colletotrichum truncatum is likely linked to CYP51A and/or CYP51B gene variants. Phytopathology, 108(11), 1263–1275. https://doi.org/10.1094/PHYTO-02-18-0054-R
Chen S.N., Luo C.X., Hu M.J., Schnabel G. (2016) Sensitivity of Colletotrichum species, including C. fioriniae and C. nymphaeae, from peach to demethylation inhibitor fungicides. Plant Disease, 100(12), 2434–2441. https://doi.org/10.1094/PDIS-04-16-0574-RE
Chung, W. H., Chung, W. C., Peng, M. T., Yang, H. R., & Huang, J. W. (2010). Specific detection of benzimidazole resistance in Colletotrichum gloeosporioides from fruit crops by PCR-RFLP. New Biotechnology, 27(1), 17–24. https://doi.org/10.1016/j.nbt.2009.10.004
Chung, W. H., 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 Disease, 90(4), 506–512. https://doi.org/10.1094/PD-90-0506
Davidse, L. C. (1973). Antimitotic activity of methyl benzimidazole-2-yl carbamate (MBC) in Aspergillus nidulans. Pesticide Biochemistry and Physiology, 3, 317–325. https://doi.org/10.1016/0048-3575(73)90030-8
de Waard, M. A., Andrade, A. C., Hayashi, K., Schoonbeek, H.-j., Stergiopoulos, I., & Zwiers, L.-H. (2006). Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Management Science, 62, 195–207. https://doi.org/10.1002/ps.1150
de Waard, M. A. (1997). Significance of ABC transporters in fungicide sensitivity and resistance. Pesticide Science, 51(3), 271–275. https://doi.org/10.1002/(SICI)1096-9063(199711)51:3%3c271::AID-PS642%3e3.0.CO;2-%23
Fan, F., Hahn, M., Li, G. Q., Lin, Y., & Luo, C. X. (2019). Rapid detection of benzimidazole resistance in Botrytis cinerea by loop-mediated isothermal amplification. Phytopathology Research, 1, 10. https://doi.org/10.1186/s42483-019-0016-8
Fernández-Ortuño, D., Grabke, A., Bryson, P. K., Amiri, A., Peres, N. A., & Schnabel, G. (2014). Fungicide resistance profiles in Botrytis cinerea from strawberry fields of seven southern U.S. states. Plant Disease, 98, 825–833. https://doi.org/10.1094/PDIS-09-13-0970-RE
Fernández-Ortuño, D., Torés, J. A., De Vicente, A., & Pérez-García, A. (2008). Mechanisms of resistance to QoI fungicides in phytopathogenic fungi. International Microbiology, 11(1), 1. https://doi.org/10.2436/20.1501.01.38
Fisher, N., & Meunier, B. (2005). Re-examination of inhibitor resistance conferred by Qo-site mutations in cytochrome b using yeast as a model system. Pest Management Science, 61(10), 973–978. https://doi.org/10.1002/ps.1066
Forcelini, B. B., Lee, S., Oliveira, M. S., & Peres, N. A. (2018a). Development of high-throughput SNP genotyping assays for rapid detection of strawberry Colletotrichum species and the G143A mutation. Phytopathology, 108(12), 1501–1508. https://doi.org/10.1094/PHYTO-04-18-0128-R
Forcelini, B. B., Rebello, C. S., Wang, N. Y., & Peres, N. A. (2018b). Fitness, competitive ability, and mutation stability of isolates of Colletotrichum acutatum from strawberry resistant to QoI fungicides. Phytopathology, 108(4), 462–468. https://doi.org/10.1094/PHYTO-09-17-0296-R
Forcelini, B. B., Seijo, T. E., Amiri, A., & Peres, N. A. (2016). Resistance in strawberry isolates of Colletotrichum acutatum from Florida to quinone-outside inhibitor fungicides. Plant Disease, 100(10), 2050–2056. https://doi.org/10.1094/PDIS-01-16-0118-RE
FRAC (Fungicide Resistance Action Committee). (2020, May). List of first confirmed cases of plant pathogenic organisms resistant to disease control agents. Retrieved August 1, 2022, from https://www.frac.info/docs/default-source/publications/list-of-resistant-plant-pathogens/list-of-first-confirmed-cases-of-plant-pathogenic-organisms-resistant-to-disease-control-agents_05_2020.pdf
Fuentes-Aragón, D., Guarnaccia, V., Rebollar-Alviter, A., Juárez-Vázquez, S. B., Aguirre-Rayo, F., & Silva-Rojas, H. V. (2020). Multilocus identification and thiophanate-methyl sensitivity of Colletotrichum gloeosporioides species complex associated with fruit with symptoms and symptomless leaves of mango. Plant Pathology, 69(6), 1125–1138. https://doi.org/10.1111/ppa.13195
Gale, G. R. (1966). Selective inhibition of deoxyribonucleic acid synthesis by salicylhydroxamic acid. Proceedings of the Society for Experimental Biology and Medicine, 122(4), 1236–1240. https://doi.org/10.3181/00379727-122-3136
Haack, S. E., Ivors, K. L., Holmes, G. J., Förster, H., & Adaskaveg, J. E. (2018). Natamycin, a new biofungicide for managing crown rot of strawberry caused by QoI-Resistant Colletotrichum acutatum. Plant Disease, 102(9), 1687–1695. https://doi.org/10.1094/PDIS-12-17-2033-RE
Han, Y. C., Zeng, X. G., Xiang, F. Y., Zhang, Q. H., Guo, C., Chen, F. Y., & Gu, Y. C. (2018). Carbendazim sensitivity in populations of Colletotrichum gloeosporioides complex infecting strawberry and yams in Hubei Province of China. Journal of Integrative Agriculture, 17(6), 1391–1400. https://doi.org/10.1016/S2095-3119(17)61854-9
Hayashi, K., Schoonbeek, H. J., & De Waard, M. A. (2002). Expression of the ABC transporter BcatrD from Botrytis cinerea reduces sensitivity to sterol demethylation inhibitor fungicides. Pesticide Biochemistry and Physiology, 73(2), 110–121. https://doi.org/10.1016/S0048-3575(02)00015-9
Hu, M. J., Grabke, A., Dowling, M. E., Holstein, H. J., & Schnabel, G. (2015). Resistance in Colletotrichum siamense from peach and blueberry to thiophanate-methyl and azoxystrobin. Plant Disease, 99(6), 806–814. https://doi.org/10.1094/PDIS-10-14-1077-RE
Hu, M., & Chen, S. (2021). Non-target site mechanisms of fungicide resistance in crop pathogens: A review. Microorganisms, 9(3), 502. https://doi.org/10.3390/microorganisms9030502
Hwang S., Kim H. R., Kim J., Park J. H., Lee S. B., Cheong S. R., & Kim, H. T. (2010). Sensitivity of Colletotrichum spp. isolated from grapes in Korea to carbendazim and the mixture of carbendazim plus diethofencarb. Plant Pathology Journal, 26(1), 49–56. https://doi.org/10.5423/PPJ.2010.26.1.049
Inada, M., Ishii, H., Chung, W. H., Yamada, T., Yamaguchi, J., & Furuta, A. (2008). Occurrence of strobilurin-resistant strains of Colletotrichum gloeosporioides (Glomerella cingulata), the causal fungus of strawberry anthracnose. Japanese Journal of Phytopathology, 74, 114–117. https://doi.org/10.3186/jjphytopath.74.114
Ishii H. (2002) DNA-based approaches for diagnosis of fungicide resistance. In Clark J.M., & Yamaguchi I. (Eds.), Agrochemical Resistance: Extent, Mechanism, and Detection (808th vol., pp.242–259) American Chemical Society.
Ishii, H., Fraaije, B. A., Sugiyama, T., Noguchi, K., Nishimura, K., Takeda, T., Amano, T., & Hollomon, D. W. (2001). Occurrence and molecular characterization of strobilurin resistance in cucumber powdery mildew and downy mildew. Phytopathology, 91(12), 1166–1171. https://doi.org/10.1094/PHYTO.2001.91.12.1166
Jayawardena, R. S., Hyde, K. D., Damm, U., Cai, L., Liu, M., Li, X. H., Zhang, W., Zhao, W. S., & Yan, J. Y. (2016). Notes on currently accepted species of Colletotrichum. Mycosphere, 7(8), 1192–1260. https://doi.org/10.5943/mycosphere/si/2c/9
Khozin-Goldberg, I., Bigogno, C., & Cohen, Z. (1999). Salicylhydroxamic acid inhibits Δ6 desaturation in the microalga Porphyridium cruentum. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 1439(3), 384–394. https://doi.org/10.1016/S1388-1981(99)00107-9
Kim, S., Park, S. Y., Kim, H., Kim, D., Lee, S. W., Kim, H. T., Lee, S., Kim, H. T., & Choi, W. (2014). Isolation and characterization of the Colletotrichum acutatum ABC transporter CaABC1. The Plant Pathology Journal, 30(4), 375. https://doi.org/10.5423/PPJ.OA.08.2014.0077
Kongtragoul, P., Nalumpang, S., Miyamoto, Y., Izumi, Y., & Akimitsu, K. (2011). Mutation at codon 198 of TUB2 gene for carbendazim resistance in Colletotrichum gloeosporioides causing mango anthracnose in Thailand. Journal of Plant Protection Research, 51(4), 377–384. https://doi.org/10.2478/v10045-011-0061-5
Leite, I. C. H. L., Silva, R. A., Santos, J. E. C. C., Freitas-Lopes, R. L., Câmara, M. P. S., Michereff, S. J., & Lopes, U. P. (2020). Analysis of Colletotrichum musae populations from Brazil reveals the presence of isolates with high competitive ability and reduced sensitivity to postharvest fungicides. Plant Pathology, 69(8), 1529–1539. https://doi.org/10.1111/ppa.13229
Liu, Z., Jian, Y., Chen, Y., Corby, K. H., He, P., Ma, Z., & Yin, Y. (2019). A phosphorylated transcription factor regulates sterol biosynthesis in Fusarium graminearum. Nature Communications, 10, 1228. https://doi.org/10.1038/s41467-019-09145-6
Luo, C. X., & Schnabel, G. (2008). The cytochrome P450 lanosterol 14α-demethylase gene is a demethylation inhibitor fungicide resistance determinant in Monilinia fructicola field isolates from Georgia. Applied and Environmental Microbiology, 74(2), 359–366. https://doi.org/10.1128/AEM.02159-07
Luo, Q., Schoeneberg, A., & Hu, M. (2020). Resistance to azoxystrobin and thiophanate-methyl is widespread in Colletotrichum spp. isolates from the Mid-Atlantic Strawberry Fields. Plant Disease, 105, 2202–2208. https://doi.org/10.1094/PDIS-09-20-2048-RE
Ma, Z., Proffer, T. J., Jacobs, J. L., & Sundin, G. W. (2006). Overexpression of the 14α-demethylase target gene (CYP51) mediates fungicide resistance in Blumeriella jaapii. Applied and Environmental Microbiology, 72(4), 2581–2585. https://doi.org/10.1128/AEM.72.4.2581-2585.2006
Marin-Felix, Y., Groenewald, J. Z., Cai, L., Chen, Q., Marincowitz, S., Barnes, I., Bensch, K., Braun, U., Camporesi, E., Damm, U., de Restrepo, Z. W., Hyde, K. D., Jayawardena, R. S., Lombard, L., & Luangsa-ard., J., … & De Beer Z.W. (2017). Genera of phytopathogenic fungi: GOPHY 1. Studies in Mycology, 86, 99–216. https://doi.org/10.1016/j.simyco.2017.04.002
Martel, C. M., Parker, J. E., Bader, O., Weig, M., Gross, U., Warrilow, A. G. S., Rolley, N., Kelly, D. E., & Kelly, S. L. (2010). Identification and characterization of four azole-resistant erg3 mutants of Candida albicans. Antimicrobial Agents and Chemotherapy, 54(11), 4527–4533. https://doi.org/10.1128/AAC.00348-10
Maymon, M., Zveibil, A., Pivonia, S., Minz, D., & Freeman, S. (2006). Identification and characterization of benomyl-resistant and-sensitive populations of Colletotrichum gloeosporioides from statice (Limonium spp.). Phytopathology, 96(5), 542–548. https://doi.org/10.1094/PHYTO-96-0542
Moreira, R. R., Hamada, N. A., Peres, N. A., & De Mio, L. L. M. (2019). Sensitivity of the Colletotrichum acutatum species complex from apple trees in Brazil to dithiocarbamates, methyl benzimidazole carbamates, and quinone outside inhibitor fungicides. Plant Disease, 103(10), 2569–2576. https://doi.org/10.1094/PDIS-07-18-1144-RE
Nakaune, R., & Nakano, M. (2007). Benomyl resistance of Colletotrichum acutatum is caused by enhanced expression of β-tubulin 1 gene regulated by putative leucine zipper protein CaBEN1. Fungal Genetics and Biology, 44(12), 1324–1335. https://doi.org/10.1016/j.fgb.2007.03.007
Nakaune, R., Adachi, K., Nawata, O., Tomiyama, M., Akutsu, K., & Hibi, T. (1998). A novel ATP-binding cassette transporter involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum. Applied and Environmental Microbiology, 64(10), 3983–3988. https://doi.org/10.1128/AEM.64.10.3983-3988.1998
Nalumpang, S., Miyamoto, Y., Miyake, C., Izumi, Y., Akitmitsu, K., & Kongtragoul, P. (2010). Point mutations in the beta-tubulin gene conferred carbendazim-resistant phenotypes of Colletotrichum gloeosporioides causing ‘Nam Dok Mai’ mango anthracnose. International Journal of Agricultural Technology, 6(2), 365–378.
Olaya, G., & Köller, W. (1999). Baseline sensitivities of Venturia inaequalis populations to the strobilurin fungicide kresoxim-methyl. Plant Disease, 83, 274–278. https://doi.org/10.1094/PDIS.1999.83.3.274
Olaya, G., Zheng, D., & Köller, W. (1998). Differential responses of germinating Venturia inaequalis conidia to kresoxim-methyl. Pesticide Science, 54, 230–236. https://doi.org/10.1002/(SICI)1096-9063(1998110)54:3%3c230::AID-PS815%3e3.0.CO;2-O
Pang, S. Y. M., Tristram, S., & Brown, S. (2010). Salicylhydroxamic acid inhibits the growth of Candida albicans. International Journal of Biological and Life Sciences, 6, 40–46.
Peres, N. A. R., Souza, N. L., Peever, T. L., & Timmer, L. W. (2004). Benomyl sensitivity of isolates of Colletotrichum acutatum and C. gloeosporioides from citrus. Plant Disease, 88, 125–130. https://doi.org/10.1094/PDIS.2004.88.2.125
Piccirillo, G., Carrieri, R., Polizzi, G., Azzaro, A., Lahoz, E., Fernández-Ortuño, D., & Vitale, A. (2018). In vitro and in vivo activity of QoI fungicides against Colletotrichum gloeosporioides causing fruit anthracnose in Citrus sinensis. Scientia Horticulturae, 236, 90–95. https://doi.org/10.1016/j.scienta.2018.03.044
Poti, T., Mahawan, K., Cheewangkoon, R., Arunothayanan, H., Akimitsu, K., & Nalumpang, S. (2020). Detection and molecular characterization of carbendazim-resistant Colletotrichum truncatum isolates causing anthracnose of soybean in Thailand. Journal of Phytopathology, 168(5), 267–278. https://doi.org/10.1111/jph.12888
Ramdial, H., Hosein, F. N., & Rampersad, S. N. (2016). Detection and molecular characterization of benzimidazole resistance among Colletotrichum truncatum isolates infecting bell pepper in Trinidad. Plant Disease, 100, 1146–1152. https://doi.org/10.1094/PDIS-09-15-0995-RE
Reimann, S., & Deising, H. B. (2005). Inhibition of efflux transporter-mediated fungicide resistance in Pyrenophora tritici-repentis by a derivative of 4′-hydroxyflavone and enhancement of fungicide activity. Applied and Environmental Microbiology, 71(6), 3269–3275. https://doi.org/10.1128/AEM.71.6.3269-3275.2005
Ren, L., Wang, S. F., Shi, X. J., Cao, J. Y., Zhou, J. B., & Zhao, X. J. (2020). Characterisation of sensitivity of Colletotrichum gloeosporioides and Colletotrichum capsici, causing pepper anthracnose, to picoxystrobin. Journal of Plant Diseases and Protection, 127, 657–666. https://doi.org/10.1007/s41348-020-00316-y
Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., & Sánchez-Gracia, A. (2017). DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution, 34(12), 3299–3302. https://doi.org/10.1093/molbev/msx248
Sato, T. (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. Transactions of the Mycological Society of Japan, 39, 35–44.
Seyran, M., Brenneman, T. B., & Stevenson, K. L. (2010). In vitro toxicity of alternative oxidase inhibitors salicylhydroxamic acid and propyl gallate on Fusicladium effusum. Journal of Pest Science, 83(4), 421–427. https://doi.org/10.1007/s10340-010-0312-7
Takushi, T., Kadekaru, K., Arasaki, C., & Taba, S. (2014). Occurrence of strobilurin-resistant strains of Colletotrichum gloeosporioides, the causal fungus of mango anthracnose. Japanese Journal of Phytopathology, 80(2), 119–123. https://doi.org/10.3186/jjphytopath.80.119
Torres-Calzada, C., Tapia-Tussell, R., Higuera-Ciapara, I., Martin-Mex, R., Nexticapan-Garcez, A., & Perez-Brito, D. (2015). Sensitivity of Colletotrichum truncatum to four fungicides and characterization of thiabendazole-resistant isolates. Plant Disease, 99(11), 1590–1595. https://doi.org/10.1094/PDIS-11-14-1183-RE
Vela-Corcía, D., Romero, D., de Vicente, A., & Pérez-García, A. (2018). Analysis of β-tubulin-carbendazim interaction reveals that binding site for MBC fungicides does not include residues involved in fungicide resistance. Scientific Reports, 8, 7161. https://doi.org/10.1038/s41598-018-25336-5
Vieira, W. A. S., Lima, W. G., Nascimento, E. S., Michereff, S. J., Reis, A., Doyle, V. P., & Câmara, M. P. S. (2017). Thiophanate-methyl resistance and fitness components of Colletotrichum musae isolates from banana in Brazil. Plant Disease, 101(9), 1659–1665. https://doi.org/10.1094/PDIS-11-16-1594-RE
Vincelli, P. (2002). QoI (Strobilurin) Fungicides: Benefits and Risks. The Plant Health Instructor. https://doi.org/10.1094/PHI-I-2002-0809-02
Wang, J., Shi, D., Wei, L., Chen, W., Ma, W., Chen, C., & Wang, K. (2020). Mutations at sterol 14α-demethylases (CYP51A&B) confer the DMI resistance in Colletotrichum gloeosporioides from grape. Pest Management Science, 76(12), 4093–4103. https://doi.org/10.1002/ps.5964
Wei, L. L., Chen, W. C., Zhao, W. C., Wang, J., Wang, B. R., Li, F. J., Wei, M.-d, Guo, J., Chen, C., Zheng, J., & Wang, K. (2020). Mutations and overexpression of CYP51 associated with DMI-resistance in Colletotrichum gloeosporioides from Chili. Plant Disease, 104(3), 668–676. https://doi.org/10.1094/PDIS-08-19-1628-RE
Wei, L., Zheng, H., Zhang, P., Chen, W., Zheng, J., Chen, C., & Cao, A. (2021). Molecular and biochemical characterization of Colletotrichum gloeosporioides isolates resistant to azoxystrobin from grape in China. Plant Pathology, 70, 1300–1309. https://doi.org/10.1111/ppa.13372
Wong, F. P., de la Cerda, K. A., Hernandez-Martinez, R., & Midland, S. L. (2008). Detection and characterization of benzimidazole resistance in California populations of Colletotrichum cereale. Plant Disease, 92(2), 239–246. https://doi.org/10.1094/PDIS-92-2-0239
Wong, F. P., Midland, S. L., & de la Cerda, K. A. (2007). Occurrence and distribution of QoI-resistant isolates of Colletotrichum cereale from annual bluegrass in California. Plant Disease, 91(12), 1536–1546. https://doi.org/10.1094/PDIS-91-12-1536
Wood, P. M., & Hollomon, D. W. (2003). A critical evaluation of the role of alternative oxidase in the performance of strobilurin and related fungicides acting at the Qo site of complex III. Pest Management Science, 59(5), 499–511. https://doi.org/10.1002/ps.655
Wu, J. Y., Hu, X. R., & Zhang, C. Q. (2019). Molecular detection of QoI resistance in Colletotrichum gloeosporioides causing strawberry anthracnose based on loop-mediated isothermal amplification assay. Plant Disease, 103(6), 1319–1325. https://doi.org/10.1094/PDIS-09-18-1593-RE
Yang, H., Tong, J., Lee, C. W., Ha, S., Eom, S. H., & Im, Y. J. (2015). Structural mechanism of ergosterol regulation by fungal sterol transcription factor Upc2. Nature Communications, 6(1), 1–13. https://doi.org/10.1038/ncomms7129
Yano, K., Ishii, H., Fukaya, M., Kawada, Y., & Sato, T. (2004). Anthracnose on Japanese pear caused by intermediately benzimidazole-resistant strains of Colletotrichum gloeosporioides (Glomerella cingulata). Japanese Journal of Phytopathology, 70, 314–319. https://doi.org/10.3186/jjphytopath.70.314
Yokosawa, S., Eguchi, N., Kondo, K. I., & Sato, T. (2017). Phylogenetic relationship and fungicide sensitivity of members of the Colletotrichum gloeosporioides species complex from apple. Journal of General Plant Pathology, 83, 291–298. https://doi.org/10.1007/s10327-017-0732-9
Young, J. R., Tomaso-Peterson, M., de la Cerda, K., & Wong, F. P. (2010a). Two mutations in β-tubulin 2 gene associated with thiophanate-methyl resistance in Colletotrichum cereale isolates from creeping bentgrass in Mississippi and Alabama. Plant Disease, 94(2), 207–212. https://doi.org/10.1094/PDIS-94-2-0207
Young, J. R., Tomaso-Peterson, M., Tredway, L. P., & de la Cerda, K. (2010b). Occurrence and molecular identification of azoxystrobin-resistant Colletotrichum cereale isolates from golf course putting greens in the southern United States. Plant Disease, 94(6), 751–757. https://doi.org/10.1094/PDIS-94-6-0751
Zhang, C., Diao, Y., Wang, W., Hao, J., Imran, M., Duan, H., & Liu, X. (2017). Assessing the risk for resistance and elucidating the genetics of Colletotrichum truncatum that is only sensitive to some DMI fungicides. Frontiers in Microbiology, 8, 1779. https://doi.org/10.3389/fmicb.2017.01779
Zhong, S., Miao, J., Liu, X., & Zhang, G. (2020). Characterization of Colletotrichum spp. sensitivity to carbendazim for isolates causing strawberry anthracnose in China. Plant Disease, 105, 87–95. https://doi.org/10.1094/PDIS-04-20-0875-RE
Acknowledgements
The authors thank the Institute of Plant Breeding, College of Agriculture and Food Science, University of the Philippines Los Baños and the Department of Science and Technology-Philippine Council for Agriculture, Aquatic and Natural Resources Research and Development (DOST-PCAARRD) for continued support. The authors also thank Dr. Maria Luz J. Sison for the assistance in proofreading the manuscript.
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Cris Q. Cortaga and Benjamine William P. Cordez- conceptualization, design, data analysis, and manuscript drafting; Leilani S. Dacones- design, supervision, review, and editing; Mark Angelo O. Balendres and Fe M. Dela Cueva- supervision, review, and editing. The authors have read and approved the final manuscript for publication.
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Cortaga, C.Q., Cordez, B.W.P., Dacones, L.S. et al. Mutations associated with fungicide resistance in Colletotrichum species: A Review. Phytoparasitica 51, 569–592 (2023). https://doi.org/10.1007/s12600-023-01063-0
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DOI: https://doi.org/10.1007/s12600-023-01063-0