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Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance

Nature Genetics volume 50, pages 375–380 (2018)Cite this article

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Abstract

Host resistance and fungicide treatments are cornerstones of plant-disease control. Here, we show that these treatments allow sex and modulate parenthood in the fungal wheat pathogen Zymoseptoria tritici. We demonstrate that the Z. tritici–wheat interaction complies with the gene-for-gene model by identifying the effector AvrStb6, which is recognized by the wheat resistance protein Stb6. Recognition triggers host resistance, thus implying removal of avirulent strains from pathogen populations. However, Z. tritici crosses on wheat show that sex occurs even with an avirulent parent, and avirulence alleles are thereby retained in subsequent populations. Crossing fungicide-sensitive and fungicide-resistant isolates under fungicide pressure results in a rapid increase in resistance-allele frequency. Isolates under selection always act as male donors, and thus disease control modulates parenthood. Modeling these observations for agricultural and natural environments reveals extended durability of host resistance and rapid emergence of fungicide resistance. Therefore, fungal sex has major implications for disease control.

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Fig. 1: Cloning of AvrStb6 in Z. tritici isolate IPO323.
Fig. 2: Sex in Z. tritici.
Fig. 3: Inoculation and mating/competition assays with Z. tritici.
Fig. 4: Comparison of the EPP model and Leonard’s model in an agricultural and natural scenario.

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Acknowledgements

We acknowledge financial support from the Sixth EU Framework Programme (BioExploit-EU FP6) Food Quality and Safety priority (contract no. 513959 to G.H.J.K. and E.C.P.V.); the Dutch Ministry of Agriculture, Nature and Food Quality; Bayer CropScience; Monsanto’s Beachell-Borlaug International Scholars Program (3340030501 to L.A.); the L’Oréal-UNESCO For Women in Science Fellowship (ERI/RPO/PPF/CDC/10.299 to S.B.M.); the Consejo Nacional de Ciencia y Tecnología, Mexico (CONACyT, no. 87781 to C.D.-T.); the Netherlands Organization for Scientific Research (NWO-VENI 863.15.005 to M.F.S.; NWO-VICI 865.11.003 to B.P.H.J.T.); and the Dioraphte Foundation (14.03.01.00 to H.J.G.M. and G.H.J.K.). We thank O. Mendes, I. de Vries, and C. van Schaik for general support, and B. A. McDonald (ETH, Plant Pathology, Zürich, Switzerland) for sharing unpublished results.

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Author notes

  1. Amir Mirzadi Gohari

    Present address: Department of Plant Protection, College of Agriculture, University of Tehran, Karaj, Iran

  2. Sarah B. Ware

    Present address: Department of Biological Sciences, Benedictine University, Lisle, IL, USA

  3. These authors contributed equally: Gerrit H. J. Kema, Amir Mirzadi Gohari, Lamia Aouini and Hesham A. Y. Gibriel.

Authors and Affiliations

  1. Wageningen Plant Research, Wageningen University and Research, Wageningen, the Netherlands

    Gerrit H. J. Kema, Amir Mirzadi Gohari, Lamia Aouini, Sarah B. Ware, Caucasella Diaz-Trujillo, Henk J. Schouten, Theo A. J. van der Lee, Cees Waalwijk, Els C. P. Verstappen & Harold J. G. Meijer

  2. Laboratory of Phytopathology, Wageningen University and Research, Wageningen, the Netherlands

    Gerrit H. J. Kema, Hesham A. Y. Gibriel, Caucasella Diaz-Trujillo, Maarten A. de Waard, Pierre J. G. M. de Wit, Bart P. H. J. Thomma & Michael F. Seidl

  3. Rothamsted Research, Harpenden, UK

    Frank van den Bosch, Robbie Manning-Smith, Vasthi Alonso-Chavez & Joe Helps

  4. Laboratory of Molecular Plant Physiology, Biotechnology Center of Borj Cedria (CBBC), Hammam-Lif, Tunisia

    Sarrah Ben M’Barek

  5. Department of Agricultural Biotechnology, College of Agriculture, Isfahan University of Technology, Isfahan, Iran

    Rahim Mehrabi

  6. Department of Plant Pathology, Tarbiat Modares University, Tehran, Iran

    Elham Zamani

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  1. Gerrit H. J. Kema
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Contributions

G.H.J.K., P.J.G.M.d.W., B.P.H.J.T., M.F.S., M.A.d.W., and C.W. designed the study. S.B.W., S.B.M., C.D.-T., E.Z., L.A., and E.C.P.V. performed the crossing assays and collected and analyzed the genotypic and phenotypic data. T.A.J.v.d.L., H.J.S., and L.A. generated the genetic linkage maps, and H.J.S. and L.A. fine mapped AvrStb6. L.A., A.M.G., H.A.Y.G., R.M., and H.J.G.M. performed AvrStb6 candidate analyses and additional genome analyses, and A.M.G. and L.A. performed the functional analysis of AvrStb6. H.A.Y.G. and M.F.S. analyzed the genomic sequences and reannotated the IPO323 and IPO94269 genome sequence. G.H.J.K. and F.v.d.B. conceptualized the EPP model, and F.v.d.B., R.M.-S., V.A.-C., and J.H. mathematically developed the EPP model. G.H.J.K. wrote the paper with substantial input from S.B.W., B.P.H.J.T., H.J.G.M., M.F.S., F.v.d.B., and J.H. G.H.J.K. coordinated the project.

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Kema, G.H.J., Mirzadi Gohari, A., Aouini, L. et al. Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance. Nat Genet 50, 375–380 (2018). https://doi.org/10.1038/s41588-018-0052-9

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