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Yeast community associated with winter wheat leaves and its sensitivity to fungicides

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Abstract

Microbial communities inhabiting the plant phyllosphere play an important role in plant health, yet their responses to agricultural chemicals remain understudied. Understanding the effect of fungicides is crucial for developing sustainable disease management strategies that preserve beneficial microbial diversity alongside effective pathogen control. This study aimed to characterise the yeast community associated with winter wheat leaves and to assess its sensitivity to fungicides used in conventional agriculture. A total of 34 yeast species were identified from 454 isolates, with 98% belonging to the phylum Basidiomycota. Sporobolomyces roseus was the dominant species, while Vishniacozyma spp. and Rhodotorula babjevae were also frequent. During the vegetation period, the abundance of three species exhibited temporal variation. Fungicide sensitivity profiling revealed that non-target yeasts were more sensitive than Zymoseptoria tritici, the pathogen responsible for septoria tritici blotch, to commonly applied fungicides such as mefentrifluconazole, prothioconazole-desthio, pyraclostrobin, and azoxystrobin. In contrast, fenpicoxamid exhibited the lowest off-target effect while remaining highly active against Z. tritici. These findings highlight the ecological complexity of the wheat phyllosphere and the potential unintended consequences of fungicide use.

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Data availability

All data generated or analysed during this study are included in this published article and its Supplementary Information files. The 5.8S-ITS sequences of yeast strains were deposited in the GenBank database under the accession numbers PV682894 to PV682927.

References

  1. FAOSTAT www.fao.org.

  2. Kavamura, V. N., Mendes, R., Bargaz, A. & Mauchline, T. H. Defining the wheat microbiome: towards microbiome-facilitated crop production. Comput. Struct. Biotechnol. J. 19, 1200–1213. https://doi.org/10.1016/j.csbj.2021.01.045 (2021).

    Google Scholar 

  3. Karlsson, I., Friberg, H., Steinberg, C. & Persson, P. Fungicide effects on fungal community composition in the wheat phyllosphere. PLoS ONE 9, e111786. https://doi.org/10.1371/journal.pone.0111786 (2014).

    Google Scholar 

  4. Sapkota, R., Jorgensen, L. N. & Nicolaisen, M. Spatiotemporal variation and networks in the mycobiome of the wheat canopy. Front. Plant Sci. 8, 1357. https://doi.org/10.3389/fpls.2017.01357 (2017).

    Google Scholar 

  5. Knorr, K., Jorgensen, L. N. & Nicolaisen, M. Fungicides have complex effects on the wheat phyllosphere mycobiome. PLoS ONE 14, e0213176. https://doi.org/10.1371/journal.pone.0213176 (2019).

    Google Scholar 

  6. Grudzinska-Sterno, M., Yuen, J., Stenlid, J. & Djurle, A. Fungal communities in organically grown winter wheat affected by plant organ and development stage. Eur. J. Plant Pathol. 146, 401–417. https://doi.org/10.1007/s10658-016-0927-5 (2016).

    Google Scholar 

  7. Gouka, L., Vogels, C., Hansen, L. H., Raaijmakers, J. M. & Cordovez, V. Genetic, phenotypic and metabolic diversity of yeasts from wheat flag leaves. Front. Plant Sci. 13, 908628. https://doi.org/10.3389/fpls.2022.908628 (2022).

    Google Scholar 

  8. Sapkota, R., Knorr, K., Jørgensen, L. N., O’Hanlon, K. A. & Nicolaisen, M. Host genotype is an important determinant of the cereal phyllosphere mycobiome. New Phytol. 207, 1134–1144. https://doi.org/10.1111/nph.13418 (2015).

    Google Scholar 

  9. Goodwin, B. S. Diseases affecting wheat: Septoria tritici blotch. In Integrated disease management of wheat and barley (ed. Oliver, R.) 47–68 (Burleigh Dodds Science Publishing, 2018).

    Google Scholar 

  10. Fones, H. & Gurr, S. The impact of septoria tritici blotch disease on wheat: An EU perspective. Fungal Genet. Biol. 79, 3–7. https://doi.org/10.1016/j.fgb.2015.04.004 (2015).

    Google Scholar 

  11. Mäe, A., Fillinger, S., Sooväli, P. & Heick, T. M. Fungicide sensitivity shifting of Zymoseptoria tritici in the finnish-baltic region and a novel insertion in the MFS1 promoter. Front. Plant Sci. 11, 385. https://doi.org/10.3389/fpls.2020.00385 (2020).

    Google Scholar 

  12. Jorgensen, L. N. et al. IPM Strategies and their dilemmas including an introduction to www.eurowheat.org. J Integr Agr 13, 265-281, https://doi.org/10.1016/S2095-3119(13)60646-2 (2014).

  13. Orton, E. S., Deller, S. & Brown, J. K. Mycosphaerella graminicola: from genomics to disease control. Mol. Plant Pathol. 12, 413–424. https://doi.org/10.1111/j.1364-3703.2010.00688.x (2011).

    Google Scholar 

  14. Jørgensen, L. N. et al. Decreasing azole sensitivity of Z tritici in Europe contributes to reduced and varying field efficacy. J Plant Dis Protect 128, 287-301, https://doi.org/10.1007/s41348-020-00372-4 (2021).

  15. Ziogas, B. N. & Malandrakis, A. A. Sterol Biosynthesis Inhibitors: C14 Demethylation (DMIs). In Fungicide Resistance in Plant Pathogens: Principles and a Guide to Practical Management (eds Hideo Ishii & Derek William Hollomon) 199-216 (Springer Japan, Tokyo, 2015).

  16. Bouillaud, F. Inhibition of Succinate Dehydrogenase by Pesticides (SDHIs) and Energy Metabolism. Int J Mol Sci 24, https://doi.org/10.3390/ijms24044045 (2023).

  17. Bartlett, D. W. et al. The strobilurin fungicides. Pest Manag Sci 58, 649–662. https://doi.org/10.1002/ps.520 (2002).

    Google Scholar 

  18. Owen, W. J. et al. Biological characterization of fenpicoxamid, a new fungicide with utility in cereals and other crops. Pest Manag Sci 73, 2005–2016. https://doi.org/10.1002/ps.4588 (2017).

    Google Scholar 

  19. Kildea, S. et al. Prevalence of key resistance alleles associated with DMI and SDHI fungicide resistance in European populations in 2022. J Plant Dis Protect 132, https://doi.org/10.1007/s41348-024-01049-y (2025).

  20. Jorgensen, L. N. & Heick, T. M. Azole Use in Agriculture, Horticulture, and Wood Preservation – Is It Indispensable?. Front Cell Infect Microbiol 11, 730297. https://doi.org/10.3389/fcimb.2021.730297 (2021).

    Google Scholar 

  21. Jorgensen, L. N. et al. Shifting sensitivity of septoria tritici blotch compromises field performance and yield of main fungicides in Europe. Front Plant Sci 13, 1060428. https://doi.org/10.3389/fpls.2022.1060428 (2022).

    Google Scholar 

  22. Kiiker, R., Juurik, M., Heick, T. M. & Mäe, A. Changes in DMI, SDHI, and QoI Fungicide Sensitivity in the Estonian Zymoseptoria tritici Population between 2019 and 2020. Microorganisms 9, https://doi.org/10.3390/microorganisms9040814 (2021).

  23. Lavrukaite, K., Heick, T. M., Ramanauskiene, J., Armoniene, R. & Ronis, A. Fungicide sensitivity levels in the Lithuanian Zymoseptoria tritici population in 2021. Front Plant Sci 13, 1075038. https://doi.org/10.3389/fpls.2022.1075038 (2022).

    Google Scholar 

  24. Zhang, J. et al. Evolution of cross-resistance to medical triazoles in Aspergillus fumigatus through selection pressure of environmental fungicides. Proc Biol Sci https://doi.org/10.1098/rspb.2017.0635 (2017).

  25. Bastos, R. W., Rossato, L., Goldman, G. H. & Santos, D. A. Fungicide effects on human fungal pathogens: Cross-resistance to medical drugs and beyond. PLoS Pathog. 17, e1010073. https://doi.org/10.1371/journal.ppat.1010073 (2021).

    Google Scholar 

  26. Castelo-Branco, D. et al. Collateral consequences of agricultural fungicides on pathogenic yeasts: a one health perspective to tackle azole resistance. Mycoses 65, 303–311. https://doi.org/10.1111/myc.13404 (2022).

    Google Scholar 

  27. Taxvig, C. et al. Endocrine-disrupting activities in vivo of the fungicides tebuconazole and epoxiconazole. Toxicol. Sci. 100, 464–473. https://doi.org/10.1093/toxsci/kfm227 (2007).

    Google Scholar 

  28. Draskau, M. K. & Svingen, T. Azole fungicides and their endocrine disrupting properties: perspectives on sex hormone-dependent reproductive development. Front. Toxicol. 4, 883254. https://doi.org/10.3389/ftox.2022.883254 (2022).

    Google Scholar 

  29. Kristjuhan, A., Kristjuhan, K. & Tamm, T. Richness of yeast community associated with apple fruits in Estonia. Heliyon 10, e27885. https://doi.org/10.1016/j.heliyon.2024.e27885 (2024).

    Google Scholar 

  30. Zheng, Y. et al. The assembly of wheat-associated fungal community differs across growth stages. Appl. Microbiol. Biotechnol. 105, 7427–7438. https://doi.org/10.1007/s00253-021-11550-1 (2021).

    Google Scholar 

  31. Buck, J. W. & Burpee, L. L. The effects of fungicides on the phylloplane yeast populations of creeping bentgrass. Can. J. Microbiol. 48, 522–529. https://doi.org/10.1139/w02-050 (2002).

    Google Scholar 

  32. Cordero-Bueso, G., Arroyo, T. & Valero, E. A long term field study of the effect of fungicides penconazole and sulfur on yeasts in the vineyard. Int. J. Food Microbiol. 189, 189–194. https://doi.org/10.1016/j.ijfoodmicro.2014.08.013 (2014).

    Google Scholar 

  33. Wachowska, U., Irzykowski, W. & Jedryczka, M. Agrochemicals: Effect on genetic resistance in yeasts colonizing winter wheat kernels. Ecotoxicol. Environ. Saf. 162, 77–84. https://doi.org/10.1016/j.ecoenv.2018.06.042 (2018).

    Google Scholar 

  34. Debode, J., Van Hemelrijck, W., Creemers, P. & Maes, M. Effect of fungicides on epiphytic yeasts associated with strawberry. Microbiologyopen 2, 482–491. https://doi.org/10.1002/mbo3.85 (2013).

    Google Scholar 

  35. Kildea, S., Hellin, P., Heick, T. M. & Hutton, F. Baseline sensitivity of European Zymoseptoria tritici populations to the complex III respiration inhibitor fenpicoxamid. Pest Manag Sci 78, 4488–4496. https://doi.org/10.1002/ps.7067 (2022).

    Google Scholar 

  36. Hawkins, N. J. & Fraaije, B. A. Fitness penalties in the evolution of fungicide resistance. Annu. Rev. Phytopathol. 56, 339–360. https://doi.org/10.1146/annurev-phyto-080417-050012 (2018).

    Google Scholar 

  37. Tamm, T. & Kristjuhan, A. Protocol for rapid and cost-effective extraction of genomic DNA from a wide range of wild yeast species for use in PCR-based applications. STAR Protoc. 5, 103282. https://doi.org/10.1016/j.xpro.2024.103282 (2024).

    Google Scholar 

  38. White, T. J., Bruns, T., Lee, S. & Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols A Guide to Methods and Applications (eds. Innis MA, Gelfand DH, Sninsky JJ, White TJ) 315-322 (Academic Press, London, 1990).

  39. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2 (1990).

    Google Scholar 

  40. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–1797. https://doi.org/10.1093/nar/gkh340 (2004).

    Google Scholar 

  41. Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549. https://doi.org/10.1093/molbev/msy096 (2018).

    Google Scholar 

  42. Tamura, K. & Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023 (1993).

    Google Scholar 

  43. Colwell, R. K. & Elsensohn, J. E. EstimateS turns 20: statistical estimation of species richness and shared species from samples, with non-parametric extrapolation. Ecography 37, 609–613. https://doi.org/10.1111/ecog.00814 (2014).

    Google Scholar 

  44. Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x (1948).

    Google Scholar 

  45. Pielou, E. C. The measurement of diversity in different types of biological collections. J. Theor. Biol. 13, 131–144. https://doi.org/10.1016/0022-5193(66)90013-0 (1966).

    Google Scholar 

  46. Hammer, O., Harper, D. & Ryan, P. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9 (2001).

    Google Scholar 

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Acknowledgements

This work was supported by the European Union and Estonian Research Council via project TEM-TA3 and by the Estonian Research Council (grants PSG827 to R.K. and PRG1741 to T.T.) The research is conducted using the research infrastructure “Experimental Studies and Applications of Cellular Processes – RAKERA” funded by the Estonian Research Council (TARISTU24-TK14).

Funding

This work was supported by the European Union and Estonian Research Council via project TEM-TA3 and by the Estonian Research Council (grants PSG827 to R.K. and PRG1741 to T.T.). The research is conducted using the research infrastructure “Experimental Studies and Applications of Cellular Processes – RAKERA” funded by the Estonian Research Council (TARISTU24-TK14).

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Authors and Affiliations

  1. Institute of Molecular and Cell Biology, University of Tartu, Riia 23B, 51010, Tartu, Estonia

    Helena Randmäe, Kersti Kristjuhan, Tiina Tamm & Arnold Kristjuhan

  2. Centre of Estonian Rural Research and Knowledge, 48309, Jõgeva Township, Estonia

    Regina Pütsepp, Lee Põllumaa, Kersti Lilleväli, Andres Mäe & Riinu Kiiker

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  1. Helena Randmäe
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Contributions

Conceptualization: AK, TT Formal analysis: LP, RK, AK, TT Investigation: HR, RP, LP, KK, KL, AM, RK, AK, TT Visualization: HR, LP, RK, AK, TT Writing original draft: RK, AK, TT Writing review and editing: HR, RP, LP, KK, KL, AM, RK, AK, TT

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Tiina Tamm or Arnold Kristjuhan.

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Randmäe, H., Pütsepp, R., Põllumaa, L. et al. Yeast community associated with winter wheat leaves and its sensitivity to fungicides.
Sci Rep (2026). https://doi.org/10.1038/s41598-026-38648-8

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  • DOI: https://doi.org/10.1038/s41598-026-38648-8

Keywords

  • Yeast biodiversity
  • Winter wheat
  • Agroecosystems
  • Septoria tritici blotch
  • Fungicide sensitivity profiling

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