Skip to main content
Log in

Sensitivity to tebuconazole and carbendazim in Fusarium graminearum species complex populations causing wheat head blight in southern Brazil

  • Original Article
  • Published:
Tropical Plant Pathology Aims and scope Submit manuscript

Abstract

Field trials where fungicides have been applied for Fusarium head blight (FHB) control were established and monitored in 17 municipalities in the Guarapuava region, Southern Paraná, Brazil, during four years (2011 to 2014). A total of 227 isolates belonging to the Fusarium graminearum species complex were obtained from symptomatic wheat heads. The majority of the 227 isolates (64%) were of the 15-(A)cetyl-deoxynivalenol (DON), 29% of the nivalenol (NIV) and 4% of the 3-ADON genotype. A random sample of 35 isolates was selected to determine the effective concentration of tebuconazole and carbendazim that reduces 50% of the mycelial growth (EC50). The estimated means of the EC50 ranged from 0.0004 to 3.0 and from 0.91 to 2.65 μg/ml for tebuconazole and carbendazim, respectively. Isolates of the 15-ADON genotype were less sensitive to tebuconazole compared to NIV + 3ADON. Evidence of lower sensitivity for both fungicides were detected. Discriminatory doses (carbendazim = 1.4 μg/ml and tebuconazole = 2.0 μg/ml) were used to screen the entire population (n = 227) for less-sensitive isolates. In the 2011–2014 population, four tebuconazole-less sensitive (2%) and nine carbendazim-less sensitive (4%) isolates were found, all originating from Guarapuava. A contemporary sample of isolates from 2018 to 2020 (n = 42) obtained from the same region were screened using the discriminatory doses. The frequency of the less-sensitive isolates increased over time from 2 and 4% to 24 and 95% for tebuconazole and carbendazim, respectively. Control efficacy was generally lower in plants inoculated with less-sensitive isolates. Greater number of less-sensitive individuals were recovered from plants inoculated with a mixture with a sensitive isolate and sprayed with either fungicide. The presence of less sensitive isolates suggest that selection may be associated with the frequent reports of decline in control efficacy for both fungicides tested in this study.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data and R codes used for the analysis of the data are available at: https://doi.org/10.17605/OSF.IO/6AZSN

References

  • Andrade SMP, Augusti GR, Paiva GF, Feksa HR, Tessmann DJ, Machado FJ, Mizubuti ESG, Del Ponte E (2022) Phenotypic and molecular characterization of the resistance to azoxystrobin and pyraclostrobin in Fusarium graminearum populations from Brazil. Plant Pathology 71:1152–1163

    Article  CAS  Google Scholar 

  • Arnhold E (2013) Package in the R environment for analysis of variance and complementary analyses. Brazilian Journal of Veterinary Research and Animal Science 50:488–492

    Article  Google Scholar 

  • Astolfi P, Reynoso MM, Ramirez ML, Chulze SN, Alves TCA, Tessmann DJ, Del Ponte EM (2012) Genetic population structure and trichothecene genotypes of Fusarium graminearum isolated from wheat in southern Brazil. Plant Pathology 61:289–295

    Article  CAS  Google Scholar 

  • Astolfi P, dos Santos J, Schneider L, Gomes LB, Silva CN, Tessmann DJ, Del Ponte EM (2011) Molecular survey of trichothecene genotypes of Fusarium graminearum species complex from barley in Southern Brazil. International Journal of Food Microbiology 148:197–201

    CAS  PubMed  Google Scholar 

  • Avozani A, Reis EM, Tonin RB (2014a) In vitro sensitivity reduction of Fusarium graminearum to DMI and QoI fungicides. Summa Phytopathologica 40:358–364

    Article  Google Scholar 

  • Avozani A, Tonin RB, Reis EM, Camera J, Ranzi C (2014b) In vitro sensitivity of Fusarium graminearum isolates to fungicides. Summa Phytopathologica 40:231–247

    Article  Google Scholar 

  • Becher R, Hettwer U, Karlovsky P, Deising HB, Wirsel SGR (2010) Adaptation of Fusarium graminearum to tebuconazole yielded descendants diverging for levels of fitness, fungicide resistance, virulence, and mycotoxin production. Phytopathology 100:444–453

    Article  CAS  PubMed  Google Scholar 

  • Blandino M, Minelli L, Reyneri A (2006) Strategies for the chemical control of Fusarium head blight: Effect on yield, alveographic parameters and deoxynivalenol contamination in winter wheat grain. European Journal of Agronomy 25:193–201

    Article  CAS  Google Scholar 

  • Bolanos-Carriel C, Wegulo SN, Baenziger PS, Funnell-Harris D, Hallen-Adams HE, Eskridge KM (2020) Effects of fungicide chemical class, fungicide application timing, and environment on Fusarium head blight in winter wheat. European Journal of Plant Pathology 158:667–679

    Article  CAS  Google Scholar 

  • Chen C, Wang J, Luo Q, Yuan S, Zhou M (2007) Characterization and fitness of carbendazim-resistant strains of Fusarium graminearum (wheat scab). Pest Management Science 63:1201–1207

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Zhang A-F, Gao T-C, Zhang Y, Wang W-X, Ding K-J, Chen L, Sun Z, Fang X-Z, Zhou M-G (2012) Integrated Use of pyraclostrobin and epoxiconazole for the control of Fusarium head blight of wheat in Anhui province of China. Plant Disease 96:1495–1500

    Article  CAS  PubMed  Google Scholar 

  • De Mendiburu F, Simon R (2015) Agricolae-Ten years of an open source statistical tool for experiments in breeding, agriculture and biology. PeerJ PrePrints 3:e1404v1. https://doi.org/10.7287/peerj.preprints.1404v1

  • Del Ponte EM, Garda-Buffon J, Badiale-Furlong E (2012) Deoxynivalenol and nivalenol in commercial wheat grain related to Fusarium head blight epidemics in southern Brazil. Food Chemistry 132:1087–1091

    Article  Google Scholar 

  • Del Ponte EM, Spolti P, Ward TJ, Gomes LB, Nicolli CP, Kuhnem PR, Silva CN, Tessmann DJ (2015) Regional and field-specific factors affect the composition of Fusarium head blight pathogens in subtropical no-till wheat agroecosystem of Brazil. Phytopathology 105:246–254

    Article  PubMed  Google Scholar 

  • Duffeck MR, Alves KS, Machado FJ, Esker PD, Del Ponte EM (2020) Modeling yield losses and fungicide profitability for managing Fusarium head blight in Brazilian spring wheat. Phytopathology 110:370–378

    Article  CAS  PubMed  Google Scholar 

  • Feksa HR, Do Couto HTZ, Garozi R, De Almeida JL, Gardiano CG, Tessmann DJ (2019) Pre- and post-infection application of strobilurin-triazole premixes and single fungicides for control of Fusarium head blight and deoxynivalenol mycotoxin in wheat. Crop Protection 117:128–134

    Article  CAS  Google Scholar 

  • Gomes LB, Ward TJ, Badiale-Furlong E, Del Ponte EM (2015) Species composition, toxigenic potential and pathogenicity of Fusarium graminearum species complex isolates from southern Brazilian rice. Plant Pathology 64:980–987

    Article  CAS  Google Scholar 

  • Kretschmer M, Leroch M, Mosbach A, Walker A-S, Fillinger S, Mernke D, Schoonbeek H-J, Pradier J-M, Leroux P, De Waard MA, Hahn M (2009) Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathogens 5:e1000696

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuhnem PR, Ward TJ, Silva CN, Spolti P, Ciliato ML, Tessmann DJ, Del Ponte EM (2016) Composition and toxigenic potential of the Fusarium graminearum species complex from maize ears, stalks and stubble in Brazil. Plant Pathology 65:1185–1191

    Article  CAS  Google Scholar 

  • Lehner MS, Paula Júnior TJ, Silva RA, Vieira RF, Carneiro JES, Schnabel G, Mizubuti ESG (2015) Fungicide sensitivity of Sclerotinia sclerotiorum : A thorough assessment using discriminatory dose, EC 50, high-resolution melting analysis, and description of new point mutation associated with thiophanate-methyl resistance. Plant Disease 99:1537–1543

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Fu L, Wang S, Chen J, Jiang J, Che Z, Tian Y, Chen G (2019) Carbendazim Resistance of Fusarium graminearum from Henan wheat. Plant Disease 103:2536–2540

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Yin Y, Wu J, Jiang J, Ma Z (2010) Identification and characterization of carbendazim-resistant isolates of Gibberella zeae. Plant Disease 94:1137–1142

    Article  CAS  PubMed  Google Scholar 

  • Machado FJ, de Barros AV, McMaster N, Schmale DG, Vaillancourt LJ, Del Ponte EM (2022) Aggressiveness and mycotoxin production by Fusarium meridionale compared with F. graminearum on maize ears and stalks in the field. Phytopathology 112:271–277

    Article  CAS  PubMed  Google Scholar 

  • Machado FJ, Santana FM, Lau D, Del Ponte EM (2017) Quantitative review of the effects of triazole and benzimidazole fungicides on Fusarium head blight and wheat yield in Brazil. Plant Disease 101:1633–1641

    Article  CAS  PubMed  Google Scholar 

  • Magan N, Medina A, Aldred D (2011) Possible climate-change effects on mycotoxin contamination of food crops pre- and postharvest: Mycotoxins and climate change. Plant Pathology 60:150–163

    Article  CAS  Google Scholar 

  • McCallum BD, Tekauz A, Gilbert J (2004) Barrage Zone Formation Between Vegetatively Incompatible Fusarium graminearum (Gibberella zeae) Isolates. Phytopathology 94:432–437

    Article  CAS  PubMed  Google Scholar 

  • McMullen M, Bergstrom G, De Wolf E, Dill-Macky R, Hershman D, Shaner G, Van Sanford D (2012) A unified effort to fight an enemy of wheat and barley: Fusarium Head Blight. Plant Disease 96:1712–1728

    Article  PubMed  Google Scholar 

  • Mesterházy Á, Bartók T, Lamper C (2003) Influence of wheat cultivar, species of Fusarium, and isolate aggressiveness on the efficacy of fungicides for control of Fusarium head blight. Plant Disease 87:1107–1115

    Article  PubMed  Google Scholar 

  • Mesterházy Á, Tóth B, Varga M, Bartók T, Szabó-Hevér Á, Farády L, Lehoczki-Krsjak S (2011) Role of fungicides, application of nozzle types, and the resistance level of wheat varieties in the control of Fusarium head blight and deoxynivalenol. Toxins 3:1453–1483

    Article  PubMed  PubMed Central  Google Scholar 

  • Mesterházy Á, Varga M, Tóth B, Kótai C, Bartók T, Véha A, Ács K, Vágvölgyi C, Lehoczki-Krsjak S (2018) Reduction of deoxynivalenol (DON) contamination by improved fungicide use in wheat. Part 1. Dependence on epidemic severity and resistance level in small plot tests with artificial inoculation. European Journal of Plant Pathology 151:39–55

    Google Scholar 

  • Nicolli CP, Machado FJ, Spolti P, Del Ponte EM (2018) Fitness traits of deoxynivalenol and nivalenol-producing Fusarium graminearum species complex strains from wheat. Plant Disease 102:1341–1347

    Article  CAS  PubMed  Google Scholar 

  • Nicolli CP, Spolti P, Tibola CS, Fernandes JMC, Del Ponte EM (2015) Fusarium head blight and trichothecene production in wheat by Fusarium graminearum and F. meridionale applied alone or in mixture at post-flowering. Tropical Plant Pathology 40:134–140

    Article  Google Scholar 

  • Paul PA, Bradley CA, Madden LV, Lana FD, Bergstrom GC, Dill-Macky R, Esker PD, Wise KA, McMullen M, Grybauskas A, Kirk WW, Milus E, Ruden K (2018) Meta-Analysis of the effects of QoI and DMI fungicide combinations on Fusarium head blight and deoxynivalenol in wheat. Plant Disease 102:2602–2615

    Article  CAS  PubMed  Google Scholar 

  • Paul PA, Lipps PE, Hershman DE, McMullen MP, Draper MA, Madden LV (2008) Efficacy of Triazole-Based fungicides for Fusarium head blight and deoxynivalenol control in wheat: A multivariate meta-analysis. Phytopathology 98:999–1011

    Article  CAS  PubMed  Google Scholar 

  • Pirgozliev SR, Edwards SG, Hare MC, Jenkinson P (2003) Strategies for the control of Fusarium head blight in cereals. In: Xu X, Bailey JA, Cooke BM (eds) Epidemiology of Mycotoxin Producing Fungi. Springer Netherlands, Dordrecht, 731–742

  • Qiu J, Shi J (2014) Genetic relationships, carbendazim sensitivity and mycotoxin production of the Fusarium graminearum populations from maize, wheat and rice in Eastern China. Toxins 6:2291–2309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiu J, Xu J, Shi J (2014) Molecular characterization of the Fusarium graminearum species complex in Eastern China. European Journal of Plant Pathology 139:811–823

    Article  CAS  Google Scholar 

  • R Core Team (2021) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria

  • Russell PE (2004) Sensitivity baselines in fungicide resistance research and management. FRAC Monograph, 3. CropLife International, Brussels 3:60

  • Schmale DG, Wood-Jones AK, Cowger C, Bergstrom GC, Arellano C (2011) Trichothecene genotypes of Gibberella zeae from winter wheat fields in the eastern USA. Plant Pathology 60:909–917

    Article  CAS  Google Scholar 

  • Spolti P, Barros NC, Gomes LB, dos Santos J, Del Ponte EM (2012a) Phenotypic and pathogenic traits of two species of the Fusarium graminearum complex possessing either 15-ADON or NIV genotype. European Journal of Plant Pathology 133:621–629

    Article  Google Scholar 

  • Spolti P, Del Ponte EM, Dong Y, Cummings JA, Bergstrom GC (2014) Triazole sensitivity in a contemporary population of Fusarium graminearum from New York wheat and competitiveness of a tebuconazole-resistant isolate. Plant Disease 98:607–613

    Article  CAS  PubMed  Google Scholar 

  • Spolti P, de Jorge BC, Del Ponte EM (2012b) Sensitivity of Fusarium graminearum causing head blight of wheat in Brazil to tebuconazole and metconazole fungicides. Tropical Plant Pathology 37:419–423

    Article  Google Scholar 

  • Spolti P, Del Ponte EM (2013) Agressividade diferencial de espécies do complexo Fusarium graminearum em interação com o fungicida tebuconazole na redução do rendimento de trigo. Ciência Rural 43:1569–1575

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umpiérrez-Failache M, Garmendia G, Pereyra S, Rodríguez-Haralambides A, Ward TJ, Vero S (2013) Regional differences in species composition and toxigenic potential among Fusarium head blight isolates from Uruguay indicate a risk of nivalenol contamination in new wheat production areas. International Journal of Food Microbiology 166:135–140

    Article  PubMed  Google Scholar 

  • Ward TJ, Bielawski JP, Kistler HC, Sullivan E, O’Donnell K (2002) Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proceedings of the National Academy of Sciences 99:9278–9283

    Article  CAS  Google Scholar 

  • Ward TJ, Clear RM, Rooney AP, O’Donnell K, Gaba D, Patrick S, Starkey DE, Gilbert J, Geiser DM, Nowicki TW (2008) An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genetics and Biology 45:473–484

    Article  PubMed  Google Scholar 

  • Wegulo SN, Baenziger PS, Hernandez Nopsa J, Bockus WW, Hallen-Adams H (2015) Management of Fusarium head blight of wheat and barley. Crop Protection 73:100–107

    Article  CAS  Google Scholar 

  • Wegulo SN, Bockus WW, Nopsa JH, De Wolf ED, Eskridge KM, Peiris KHS, Dowell FE (2011) Effects of integrating cultivar resistance and fungicide application on Fusarium head blight and deoxynivalenol in winter wheat. Plant Disease 95:554–560

    Article  PubMed  Google Scholar 

  • Willyerd KT, Li C, Madden LV, Bradley CA, Bergstrom GC, Sweets LE, McMullen M, Ransom JK, Grybauskas A, Osborne L, Wegulo SN, Hershman DE, Wise K, Bockus WW, Groth D, Dill-Macky R, Milus E, Esker PD, Waxman KD, Adee EA, Ebelhar SE, Young BG, Paul PA (2012) Efficacy and stability of integrating fungicide and cultivar resistance to manage Fusarium head blight and deoxynivalenol in wheat. Plant Disease 96:957–967

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Liu X, Li B, Ma Z (2009) Characterization of sterol demethylation inhibitor-resistant isolates of Fusarium asiaticum and F. graminearum collected from wheat in China. Phytopathology 99:487–497

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the Programa de Pós-graduação em Fitopatologia (UFV) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for providing a graduate scholarship to F. J. Machado and for a research fellowship for Dauri J. Tessmann, Eduardo S. G. Mizubuti and E. M. Del Ponte. We thank FAPEMIG (Fundação de Pesquisa do Estado de Minas Gerais) for the financial support (APQ—03945-16).

Author information

Authors and Affiliations

Authors

Contributions

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

Corresponding author

Correspondence to Emerson M. Del Ponte.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Machado, F.J., Silva, C.N., Paiva, G.F. et al. Sensitivity to tebuconazole and carbendazim in Fusarium graminearum species complex populations causing wheat head blight in southern Brazil. Trop. plant pathol. 49, 157–167 (2024). https://doi.org/10.1007/s40858-023-00616-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40858-023-00616-2

Keywords

Navigation