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Species diversity, resistance to MBC fungicides, and low sensitivity to azoxystrobin in field isolates of Colletotrichum spp. associated with soybean anthracnose in Mato Grosso and Goiás States, Brazil

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Abstract

The diversity of Colletotrichum species that cause soybean anthracnose results in different levels of sensitivity to the fungicides used in disease management. The inefficacy of fungicides in Brazil has already been reported, leading to losses in soybean production. This study aimed to determine the species diversity and inhibitory effects of fungicides on Colletotrichum spp. isolates associated with soybean anthracnose, and to characterize possible resistance mutations to quinone outside inhibitors (QoIs) and methyl benzimidazole carbamates (MBCs). C. plurivorum and C. musicola isolates showed low sensitivity to azoxystrobin in in vitro bioassays (EC50 > 100 μg.mL−1), while C. truncatum and C. sojae isolates were sensitive (EC50 < 50 μg.mL−1). However, only one C. musicola isolate carried the resistance mutation G143A. C. plurivorum and C. musicola isolates were resistant to thiophanate-methyl and showed the E198A mutation in the β-tub gene, whereas C. truncatum and C. sojae isolates were sensitive and lack the resistance mutation. Thus, the precise identification of the Colletotrichum species involved in the pathosystem and the monitoring of fungicide resistant isolates are urgently needed. Due to the detection of low sensitivity to azoxystrobin and resistance to thiophanate-methyl, together with the practical difficulty of identifying Colletotrichum species promptly in the field, these fungicides may not be effective in controlling anthracnose in soybean in Mato Grosso and Goiás States, Brazil. Fungicides with different modes of action should be investigated as well as anti-resistance strategies to extend the useful life of the chemicals used to control this disease.

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Data availability

All the data generated in this work is publicly available in the National Center for Biotechnology Information (NCBI) under accession numbers indicated in Table 1, Fig. 2, and Fig. 3.

References

  • Agrofit (2022) Sistema de agrotóxicos fitossanitários. In: Ministério da Agricultura Pecuária e Abastecimento. https://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed 5 Aug 2021

  • Angelini RMDM, Rotolo C, Masiello M, Pollastro S, Ishii H, Faretra F (2012) Genetic analysis and molecular characterisation of laboratory and field mutants of Botryotinia fuckeliana (Botrytis cinerea) resistant to QoI fungicides. Pest Manag Sci 68:1231–1240

    Article  Google Scholar 

  • Avila-Adame C, Olaya G, Köller W (2003) Characterization of Colletotrichum graminicola isolates resistant to strobilurin-related QoI fungicides. Plant Dis 87:1426–1432

    Article  CAS  PubMed  Google Scholar 

  • Baggio JS, Peres NA, Amorim L (2018) Sensitivity of Botrytis cinerea isolates from conventional and organic strawberry fields in Brazil to azoxystrobin, iprodione, pyrimethanil, and thiophanate-methyl. Plant Dis 102:1803–1810

    Article  CAS  PubMed  Google Scholar 

  • Barbieri MCG, Ciampi-Guillardi M, Moraes SRG, Bonaldo SM, Rogério F, Linhares RR, Massola NS (2017) First report of Colletotrichum cliviae causing anthracnose on soybean in Brazil. Plant Dis 101:1677–1677

    Article  Google Scholar 

  • Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-Dobrzanski B (2002) The strobilurin fungicides. Pest Manag Sci 58:649–662

    Article  CAS  PubMed  Google Scholar 

  • Boufleur TR, Castro RRL, Rogério F, Ciampi-Guillardi M, Baroncelli R, Massola Júnior NS (2020) First report of Colletotrichum musicola causing soybean anthracnose in Brazil. Plant Dis 104:1858

    Article  Google Scholar 

  • Boufleur TR, Ciampi-Guillardi M, Tikami Í, Rogério F, Thon MR, Sukno SA, Massola Júnior NS, Baroncelli R (2021) Soybean anthracnose caused by Colletotrichum species: current status and future prospects. Mol Plant Pathol 22:393–409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brennan GP, Fairweather I, Trudgett A, Hoey E, McCoy McConville M, Meaney M, Robinson M, McFerran N, Ryan L, Lanusse C, Mottier L, Alvarez L, Solana H, Virkel G, Brophy PM (2007) Understanding triclabendazole resistance. Exp Mol Pathol 82:104–109

    Article  CAS  PubMed  Google Scholar 

  • Brent KJ, Hollomon DW (2007) Fungicide resistance: the assessment of risk. FRAC Monograph Nr. 2. CropLife International, Brussels

  • Chechi A, Stahlecker J, Dowling ME, Schnabel G (2019) Diversity in species composition and fungicide resistance profiles in Colletotrichum isolates from apples. Pestic Biochem Physiol 158:18–24

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Wang Y, Schnabel G, Peng CA, Lagishetty S, Smith K, Luo C, Yuan H (2018) Inherent resistance to 14α-demethylation inhibitor fungicides in Colletotrichum truncatum is likely linked to CYP51A and/or CYP51B gene variants. Phytopathology 108:1263–1275

  • 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 110:615–625

  • 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 Dis 90:506–512

  • Crous PW, Groenewald JZ, Risède J-M, Simoneau P, Hywel-Jones NL (2004) Calonectria species and their Cylindrocladium anamorphs: species with sphaeropedunculate vesicles. Stud Mycol 50:415–430

  • da Silva Pesqueira A, Bacchi LMA, Gavassoni WL (2016) Associação de fungicidas no controle da antracnose da soja no Mato Grosso do Sul. Revista Ciência Agronômica 47:203–212

    Google Scholar 

  • Damm U, Sato T, Alizadeh A, Groenewald JZ, Crous PW (2019) The Colletotrichum dracaenophilum, C . magnum and C . orchidearum species complexes. Stud Mycol 92:1–46

    Article  CAS  PubMed  Google Scholar 

  • de Mello FE, Lopes-Caitar VS, Prudente H, Xavier-Valencio SA, Franzenburg S, Mehl A, Marcelino-Guimaraes FC, Verreet JA, Balbi-Peña MI, Godoy CV (2021) Sensitivity of Cercospora spp. from soybean to quinone outside inhibitors and methyl benzimidazole carbamate fungicides in Brazil. Tropical Plant Pathology 46:69–80

  • Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

  • Dias MD, Pinheiro VF, Café-Filho AC (2016) Impact of anthracnose on the yield of soybean subjected to chemical control in the north region of Brazil. Summa Phytopathol 42:18–23

  • Dias MD, Fonseca MEN, Dias-Neto JJ, Santos MDM, Pandolfo GM, Boiteux LS, Café-Filho AC (2018) Biology, pathogenicity, and haplotype analyses of Colletotrichum cliviae: a novel soybean anthracnose agent in warm tropical areas. Tropical Plant Pathology 43:439–451

  • dos Santos Vieira WA, Lima WG, Nascimento ES, Michereff SJ, Reis A, Doyle VP, Câmara MPS (2017) Thiophanate-methyl resistance and fitness components of Colletotrichum musae isolates from banana in Brazil. Plant Dis 101:1659–1665

    Article  Google Scholar 

  • Fernández-Ortuño D, Torés JA, de Vicente A, Pérez-García A (2008) Mechanisms of resistance to QoI fungicides in phytopathogenic fungi. International Microbiology 11:1–9

    PubMed  Google Scholar 

  • Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia 35:1039–1042

    Article  Google Scholar 

  • Forcelini BB, Seijo TE, Amiri A, Peres NA (2016) Resistance in strawberry isolates of Colletotrichum acutatum from Florida to quinone-outside inhibitors fungicides. Plant Disease 100:2050–2056

    Article  CAS  PubMed  Google Scholar 

  • Forcelini BB, Rebello CS, Wang N-Y, Peres NA (2018) Fitness, competitive ability, and mutation stability of isolates of Colletotrichum acutatum from strawberry resistant to QoI fungicides. Phytopathology 108:462–468

    Article  PubMed  Google Scholar 

  • Fuentes-Aragón D, Guarnaccia V, Rebollar-Alviter A, Juárez‐Vázquez SB, Aguirre‐Rayo F, Silva‐Rojas HV (2020) Multilocus identification and thiophanate-methyl sensitivity of Colletotrichum gloeosporioides species complex associated with fruit with symptoms and symptomless leaves of mango. Plant Pathol 69:1125–1138

    Article  Google Scholar 

  • Gao Y-Y, He L-F, Li B-X, Mu W, Lin J, Liu F (2017) Sensitivity of Colletotrichum acutatum to six fungicides and reduction in incidence and severity of chili anthracnose using pyraclostrobin. Australas Plant Pathol 46:521–528

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61:1323–1330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godoy CV (2011) Risk and management of fungicide resistance in the Asian soybean rust fungus Phakopsora pachyrhizi. In: Thind TS (ed) Fungicide Resistance in Crop Protection: Risk and Management. CABI Publishing, Oxfordshire, UK, pp 87–95

    Google Scholar 

  • Grasso V, Palermo S, Sierotzki H, Garibaldi A, Gisi U (2006) Cytochrome b gene structure and consequences for resistance to Qo inhibitor fungicides in plant pathogens. Pest Manag Sci 62:465–472

    Article  CAS  PubMed  Google Scholar 

  • 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 95:872–895

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Zeng X, Xiang F, Zhang Q, Guo C, Chen F, Gu Y (2018) Carbendazim sensitivity in populations of Colletotrichum gloeosporioides complex infecting strawberry and yams in Hubei Province of China. J Integr Agric 17:1391–1400

    Article  CAS  Google Scholar 

  • Hawkins NJ, Fraaije BA (2018) Fitness penalties in the evolution of fungicide resistance. Annual Review of Phytopathology 56:339–360

    Article  CAS  PubMed  Google Scholar 

  • Hu MJ, Grabke A, Dowling ME, Holstein HJ, Schnabel G (2015) Resistance in Colletotrichum siamense from peach and blueberry to thiophanate-methyl and azoxystrobin. Plant Dis 99:806–814

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Lehman SG, Wolf FA (1926) Soy-bean anthracnose. Journal of Agricultural Research 33:381–390

    Google Scholar 

  • Lucas JA, Hawkins NJ, Fraaije BA (2015) The evolution of fungicide resistance. Advances in Applied Microbiology 90:29–92

    Article  CAS  PubMed  Google Scholar 

  • Luo Q, Schoeneberg A, Hu M (2021) Resistance to azoxystrobin and thiophanate-methyl is widespread in Colletotrichum spp. isolates from the Mid-Atlantic strawberry fields. Plant Disease 105:2202–2208

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Michailides TJ (2005) Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Protection 24:853–863

    Article  CAS  Google Scholar 

  • Maddison WP, Maddison DR (2021) Mesquite: a modular system for evolutionary analysis. Version 3.70. http://www.mesquiteproject.org. Accessed 11 May 2022

  • McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology 40:349–379

    Article  CAS  PubMed  Google Scholar 

  • Munkvold GP, Watrin C, Scheller M, Zeun R, Olaya G (2014) Benefits of chemical seed treatments on crop yield and quality. Global perspectives on the health of seeds and plant propagation material. Springer, Netherlands, Dordrecht, pp 89–103

    Chapter  Google Scholar 

  • Nakata K, Takimoto K (1934) A list of crop diseases in Korea. Agriculture Experiment Station Government Central Chosen Research Report 15:1–146

    Google Scholar 

  • Neddaf HM, Aouini L, Bouznad Z, Kema GHJ (2017) Equal distribution of mating type alleles and the presence of strobilurin resistance in Algerian Zymoseptoria tritici field populations. Plant Disease 101:544–549

    Article  CAS  Google Scholar 

  • 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 . Sci Hortic 236:90–95

  • 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. J Phytopathol 168:267–278

  • Rogério F, Ciampi-Guillardi M, Barbieri MCG, Bragança CAD, Seixas CDS, Almeida AMR, Massola NS (2017) Phylogeny and variability of Colletotrichum truncatum associated with soybean anthracnose in Brazil. J Appl Microbiol 122:402–415

  • Shi NN, Ruan HC, Jie YL, Chen FR, Du YX (2021) Characterization, fungicide sensitivity and efficacy of Colletotrichum spp from chili in Fujian, China. Crop Prot 143:105572

  • Shi X-C, Wang S-Y, Duan X-C, Gao X, Zhu X-Y, Laborda P (2021) First report of Colletotrichum brevisporum causing soybean anthracnose in China. Plant Dis 105:707

  • Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38:3022–3027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Dis 99:1590–1595

    Article  CAS  PubMed  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3–new capabilities and interfaces. Nucleic Acids Res 40:e115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vielba-Fernández A, Bellón-Gómez D, Torés JA, de Vicente A, Pérez-García A, Fernández-Ortuño D (2018) Heteroplasmy for the cytochrome b gene in Podosphaera xanthii and its role in resistance to QoI fungicides in Spain. Plant Dis 102:1599–1605

    Article  PubMed  Google Scholar 

  • Wong FP, Midland SL, De La Cerda KA (2007) Occurrence and distribution of QoI-resistant isolates of Colletotrichum cereale from annual bluegrass in California. Plant Disease 91:1536–1546

    Article  CAS  PubMed  Google Scholar 

  • Wong FP, de la Cerda KA, Hernandez-Martinez R, Midland SL (2008) Detection and characterization of benzimidazole resistance in California populations of Colletotrichum cereale. Plant Disease 92:239–246

    Article  CAS  PubMed  Google Scholar 

  • Xiao K, Engstrom G, Rajagukguk S, Yu C-A, Yu L, Durham B, Millett F (2003) Effect of famoxadone on photoinduced electron transfer between the iron-sulfur center and cytochrome c1 in the cytochrome bc1 complex. J Biol Chem 278:11419–11426

  • Yang H-C, Haudenshield JS, Hartman GL (2012) First report of Colletotrichum chlorophyti causing soybean anthracnose. Plant Disease 96:1699–1699

    Article  PubMed  Google Scholar 

  • Yang H-C, Haudenshield JS, Hartman GL (2014) Colletotrichum incanum sp. nov., a curved-conidial species causing soybean anthracnose in USA. Mycologia 106:32–42

    Article  CAS  PubMed  Google Scholar 

  • Young JR, Tomaso-Peterson M, de la Cerda K, Wong FP (2010) 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 94:207–212

    Article  CAS  PubMed  Google Scholar 

  • Young JR, Tomaso-Peterson M, Tredway LP, De La Cerda K (2010) Occurrence and molecular identification of azoxystrobin-resistant Colletotrichum cereale isolates from golf course putting greens in the southern United States. Plant Disease 94:751–757

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Kim YK, Huang L, Xiao CL (2010) Resistance to thiabendazole and baseline sensitivity to fludioxonil and pyrimethanil in Botrytis cinerea populations from apple and pear in Washington State. Postharvest Biology and Technology 56:12–18

    Article  CAS  Google Scholar 

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Funding

This work was supported by the São Paulo Research Foundation (FAPESP 2017/09178–8; 2021/01606–6), National Science and Technology Development Council (CNPq 131972/2016–2 and 830702/1999–7), and National Council for the Improvement of Higher Education (PROEX/CAPES 330002037002P3).

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  1. Renata Rebellato Linhares de Castro and Maisa Ciampi-Guillardi contributed equally.

Authors and Affiliations

  1. Department of Plant Pathology and Nematology, Luiz de Queiroz College of Agriculture (ESALQ), University of São Paulo (USP), Piracicaba, SP, 13418-900, Brazil

    Renata Rebellato Linhares de Castro, Maisa Ciampi-Guillardi, Flávia Rogério, Claudio Dias da Silva Junior, Thaís Regina Boufleur & Nelson Sidnei Massola Júnior

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  1. Renata Rebellato Linhares de Castro
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  6. Nelson Sidnei Massola Júnior
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Contributions

Conceptualization: R.R.L.d.C., M.C.G., and N.S.M.Jr.; methodology: R.R.L.d.C., M.C.G., and T.R.B.; investigation: R.R.L.d.C., M.C.G., F.R., C.D.d.S.Jr., and T.R.B.; statistical analysis: R.R.L.d.C. and C.D.d.S.Jr.; writing—original draft preparation: R.R.L.d.C. and M.C.G.; writing—review and editing: T.R.B.; supervision: N.S.M.Jr. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Renata Rebellato Linhares de Castro or Nelson Sidnei Massola Júnior.

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Linhares de Castro, R.R., Ciampi-Guillardi, M., Rogério, F. et al. Species diversity, resistance to MBC fungicides, and low sensitivity to azoxystrobin in field isolates of Colletotrichum spp. associated with soybean anthracnose in Mato Grosso and Goiás States, Brazil. Trop. plant pathol. 49, 71–82 (2024). https://doi.org/10.1007/s40858-022-00547-4

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