Abstract
To control persimmon anthracnose, fungicides are applied from flowering until fruit harvest. Systemic fungicides registered for this crop are mainly from the group of quinone outside inhibitors (QoIs) and demethylation inhibitors (DMIs), both presenting risks for resistance development. For this reason, sensitivity studies and fungicide efficacy tests are important to determine the levels of sensitivity of isolates from different Colletotrichum spp. from persimmon to fungicides. The objectives of this work were: (i) to investigate the sensitivity of Colletotrichum isolates obtained from persimmon twigs and flowers to registered and non-registered active ingredients; (ii) to evaluate the cross-resistance of Colletotrichum spp. among tested fungicide groups; and (iii) to test the efficacy of fungicides in controlling anthracnose on immature and mature detached fruit. There were differences between Colletotrichum spp. in levels of sensitivity to the active ingredients evaluated, with C. horii isolates being more sensitive to site-specific fungicides than C. chrysophilum, C. nymphaeae and C. melonis. There was a high risk of cross-resistance for the active ingredients of the QoIs, medium risk for the DMIs and multisite compounds, and low risk for the succinate dehydrogenase inhibitors (SDHIs). Negative cross-resistance correlation was observed for anilopyrimidines (APs). Anthracnose control in immature and mature fruit ex vivo varied between products. In general, isolates recovered from both twigs and flowers were sensitive to the fungicides tested. The SDHI fungicides were efficient in controlling Colletotrichum in the in vitro assay, appearing as an alternative to be tested in the control of the disease. Difenoconazole-based fungicides and mixed formulations of QoI and DMI were the most effective for controlling persimmon anthracnose both for immature and mature fruit.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
AGROFIT (2022) Sistema de agrotóxicos fitossanitários. Ministério da Agricultura, Pecuária e Abastecimento. Available at: http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed on January 31, 2023
Aguiar ATE, Gonçalves C, Paterniani MEAGZ, Tucci MLS'A, de Castro CEF (2014) Instruções agrícolas para as principais culturas econômicas 7. Campinas: Instituto Agronômico p 452 (Boletim IAC, nº 200)
Amiri A, Heath SM, Peres NA (2013) Phenotypic characterization of multifungicide resistance in Botrytis cinerea isolates from strawberry fields in Florida. Plant Disease 97:393–401
Asano S, Hirayama Y (2019) Seasonal effect on infection with Colletotrichum horii causing anthracnose in persimmon twigs and the relation between its prevalence on twigs and occurrence in fruit. Annual Report of the Kansai Plant Protection Society 61:75–78
Baggio JS, Wang NY, Peres NA, 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
Box GEP, Cox DR (1964) An analysis of transformations. Journal of the Royal Statistical Society, Series B 26(2):211–252
Carraro TA, Lichtemberg PSF, Michailides TJ, Borges IM, Pereira WV, May De Mio LL (2022a) Identification and characterization of Colletotrichum species associated with anthracnose on persimmon in Brazil. Fungal Biology 126:235–249
Carraro TA, Moreira RR, Gelain J, May De Mio LL (2022b) Etiology and epidemiology of diseases caused by Colletotrichum spp. in persimmon, apple, peach, and grapevine. Revisão Anual de Patologia Plantas 28:136–162
Chen SN, Luo CX, Hu MJ, Schnabel G (2016) Sensitivity of Colletotrichum species, including C. fioriniae and C. nymphaeae, from peach to DeMethylation Inhibitor fungicides. Plant Disease 100:2434–2441
Chechi A, Stahlecker J, Dowling ME, Schnabel G (2019) Diversity in species composition and fungicide resistance profiles in Colletotrichum isolates from apples. Pesticide Biochemistry and Physiology 158:18–24
Cooper TF, Ostrowski EA, Travisano M (2007) A negative relationship between mutation pleiotropy and fitness effect in yeast. Evolution 61(6):1495–1499
da Silva LL, Moreno HLA, Correia HLN, Santana MF, de Queiroz MV (2020) Colletotrichum: species complexes, lifestyle, and peculiarities of some sources of genetic variability. Applied Microbiology Biotechnology 104(5):1891–1904
Damm U, Cannon PF, Woudenberg JHC, Crous PW (2012) The Colletotrichum acutatum species complex. Studies in Mycology 73(1):37–113
Deng Q-en, Ding X-yang, Li J-an, Cui L-kai, Xu J-qiang (2020) Morphological characteristics and genetic diversity of Colletotrichum horii infecting persimmon tree in China. European Journal of Plant Pathology 156:437–449
Dolinski MA, Carraro TA, Gorayeb ES, May De Mio LL (2022) Field studies of anthracnose symptoms and pathogen infection in different phases of the persimmon growing season. Plant Pathology 71:1120–1130
Dowling ME, Peres NA, Villani S, Schnabel G (2020) Managing Colletotrichum on Fruit Crops: A “Complex” Challenge. Plant Disease 104:2301–2316
Fernández-Ortuño D, Pérez-García A, Chamorro M, de La Peña E, de Vicente A, Torés JA (2017) Resistance to the SDHI fungicides boscalid, fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from commercial strawberry fields in Spain. Plant Disease 101(7):1306–1313
Förster H, Kanetis L, Adaskaveg JE (2004) Spiral gradient dilution, a rapid method for determining growth responses and 50% effective concentration values in fungus-fungicide interactions. Phytopathology 94(2):163–170
FRAC. Fungicide Resistance Action Committee (2022) FRAC Code List ©*2022: Fungicides sorted by mode of action (including FRAC Code numbering). Available at: <https://www.frac.info/docs/default-source/publications/frac-code-list/frac-code-list-2022--final.pdf?sfvrsn=b6024e9a_2>. Accessed on January 31, 2023
Gama AB, Baggio JS, Rebello CS, Lourenço SA, Gasparoto MC, da Silva Júnior GJ, Peres NA, Amorim L (2020) Sensitivity of Colletotrichum acutatum isolates from citrus to carbendazim, difenoconazole, tebuconazole, and trifloxystrobin. Plant Disease 104(6):1621–1628
Gang G-H, Cho HJ, Kim HS, Kwack Y-B, Kwack Y-S (2015) Analysis of fungicide sensitivity and genetic diversity among Colletotrichum species in sweet persimmon. Plant Pathology Journal 31(2):115–122
Gelain J, Lykins S, Rosa PF, Soares AT, Dowling ME, Schnabel G, May De Mio LL (2023) Identification and fungicide sensitivity of Colletotrichum spp. from apple flowers and fruitlets in Brazil. Plant Dis 107:1183–1191
Gisi U, Sierotzki H, Cook A, Maccaffery A (2002) Baseline sensitivity of Monilia yunnanensis to the DMI fungicides tebuconazole and triadimefon. European Journal of Plant Pathology 136(4):651–655
Hu M-J, Grabke A, Dowling ME, Holstein HJ, Shnabel G (2015) Resistance in Colletotrichum siamense from peach and blueberry to thiophanatemethyl and azoxystrobin. Plant Disease 99:806–814
Hu M-J, Fernández-Ortuño D, Schnabel G (2016) Monitoring resistance to SDHI fungicides in Botrytis cinerea from strawberry fields. Plant Disease 100:959–965
Ishii H, Miyamoto T, Ushiod S, Kakishimab M (2010) Lack of cross-resistance to a novel succinate dehydrogenase inhibitor, fluopyram, in highly boscalid-resistant isolates of Corynespora cassiicola and Podosphaera xanthii. Pest Management Science 67:474–482
Ishii H, Zhen F, Hu MJ, Li XP, Schnabel G (2016) Efficacy of SDHI fungicides, including benzovindiflupyr, against Colletotrichum species. Pest Management Science 72(10):1844–1853
Ishii H, Watanabe H, Yamaoka Y, Schnabel G (2022) Sensitivity to fungicides in isolates of Colletotrichum gloeosporioides and C. acutatum species complexes and efficacy against anthracnose diseases. Pesticide Biochemistry and Physiology 182:105049
Jaywardena RS, Bhunjun CS, Hyde KD, Gentekaki E, Itthayakorn P (2021) Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species. Mycosphere 12(1):519–669
Karaoglanidis GS, Thanassoulopoulos CC (2003) Cross-resistance patterns among sterol biosynthesis inhibiting fungicides (SBIs) in Cercospora beticola. European Journal of Plant Pathology 109:929–934
Lichtemberg PSF, Primiano IV, Fischer JM, Glienke C, Amorim L, May De Mio LL (2016) Resistência de Monilinia spp. aos fungicidas do grupo Inibidores da Desmetilação (IDM), Inibidores da Quinona Externa (IQe) e dos Metilo Benzimidazol Carbamatos (MBC). Revisão Anual De Patologia De Plantas 24:145–173
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. Stud Mycol 86:99–216
Moreira RR, Hamada NA, Peres NA, May De Mio LL (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 103:2569–2576
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 Disease 100:2194–2203
Pereira WV, Primiano IV, Morales RGF, Peres NA, Amorim L, May De Mio LL (2017) Reduced sensitivity to azoxystrobin of Monilinia fructicola isolates from Brazilian stone fruit is not associated with previously described mutations in the cytochrome b gene. Plant Disease 101:766–773
Schnabel G, Bryson PK, Bridges WC, Brannen PM (2004) Reduced sensitivity in Monilinia fructicola to propiconazole in Georgia and implications for disease management. Plant Disease 88(9):1000–1004
Schnabel G, Tan Q, Schneider V, Ishii H (2021) Inherent tolerance of Colletotrichum gloeosporioides to fludioxonil. Pestic Biochem Physiol 172:104767
Semar M, Strobel D, Koch A, Klappach K, Stammler G (2007) Baseline sensitivity of Monilia yunnanensis to the DMI fungicides tebuconazole and triadimefon. European Journal of Plant Pathology 136(4):651–655
Sierotzki H, Frey R, Morchoisne M, Olaya G, Mosch M, Scalliet G (2011) Sensitivity of fungal pathogens to SDHI fungicides. In: Dehne HW, Deising HB, Gisi U, Kuc, KH, Russell PE, Lyr H (Eds.) Modern fungicides and antifungal compounds. DPG, Braunschweig, Germany 6:179–186
Sierotzki H, Scalliet G (2013) A Review of Current Knowledge of Resistance Aspects for the Next-Generation Succinate Dehydrogenase Inhibitor Fungicides. Phytopathology 103(9):880–887
Stammler G, Wolf A, Glaettli A, Klappach K (2015) Respiration Inhibitors: Complex II. In: Ishii H, Hollomon D (eds) Fungicide Resistance in Plant Pathology. Springer, Tokyo, pp 105–118
Therneau TA (2020) Package for Survival Analysis in S. R package version 3.4.0. Available at: <http://CRAN.R-project.org/package=survival>. Accessed on June 21, 2020.
Torres-Londoño GA, Hausbeck M, Hao J (2016) ECX: An R Package for Studying Sensitivity of Antimicrobial Substances Using Spiral Plating Technology. Plant Healthy Progress 17(4):188–194
Weir BS, Johnston PR, Damm U (2012) The Colletotrichum gloeosporioides species complex. Studies in Mycology 73(1):115–180
Wharton PS, Diéguez-Uribeondo J (2004) The biology of Colletotrichum acutatum. Anales Del Jardín Botánico De Madrid 61(1):3–22
Yang L-N, He M-H, Ouyang H-B, Zhu W, Pan Z-C, Sui Q-J, Shang L-P, Zhan J (2019) Cross-resistance of the pathogenic fungus Alternaria alternata to fungicides with different modes of action. BMC Microbiol 19:205
Yoshimura MA, Luo Y, Ma Z, Michailides TJ (2004) Sensitivity of Monilinia fructicola from stone fruit to tiophanate-methyl, iprodione, and tebuconazole. Plant Disease 88(4):373–378
Yokosawa S, Eguchi N, Kondo K, Sato T (2017) Phylogenetic relationship and fungicide sensitivity of members of the Colletotrichum gloeosporioides species complex from apple. Journal of General Plant Pathology 83(5):291–298
Yokosawa S, Eguchi N, Sato T (2020) Characterization of the Colletotrichum gloeosporioides species complex causing grape mature rot in Nagano Prefecture, Japan. Journal of General Plant Pathology 86:163–172
Yu X, Hou C, Zhang K, Zhai H, Ma Y, Na M, Ai C (2019) Inhibitory Effect of 16 Fungicides on persimmon Anthracnose Pathogen Colletotrichum horii. Agric Biotechnol 8:31–33
Zuniga AI, Oliveira MS, Rebello C (2019) Peres NA (2019) Baseline sensitivity of Botrytis cinerea isolates from strawberry to isofetamid compared to other SDHIs. Plant Disease 104(4):1224–1230
Acknowledgements
This study was financed in part by the ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil’ (CAPES) and Finance Code 001. Co-author Louise Larissa received research fellowships from National Council for Scientific and Technological Development (CNPq)/Brazil (306907/2017-8). The authors would like to thank the laboratory team of Dr. Themis J. Michailides for excellent technical assistance, Dr. Walmes M. Zeviani for statistical analyses assistance, and Dr. Jhulia Gelain from Clemson University for assistance with English language editing.
Author information
Authors and Affiliations
Contributions
Thiago de Aguiar Carraro conducted the experiments, investigation, analyzed the data, and wrote the first draft of manuscript. Dr. Paulo dos Santos Faria Lichtemberg contributed to the study design, conceptualization, and reviewing and editing of the manuscript. Dr. Themis J. Michailides contributed to the visualization and reviewed the manuscript. Dr. Louise Larissa May De Mio contributed to the conceptualization, supervised the research, analyzed the data, and reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.
Ethics declarations
Competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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.
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
de Aguiar Carraro, T., dos Santos Faria Lichtemberg, P., Michailides, T.J. et al. Fungicide sensitivity of Colletotrichum isolates and efficacy in controlling persimmon anthracnose. Trop. plant pathol. 49, 104–119 (2024). https://doi.org/10.1007/s40858-023-00594-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40858-023-00594-5