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Host and pathogen genetics reveal an inverse gene-for-gene association in the P. teres f. maculata–barley pathosystem

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Abstract

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Pathogen and host genetics were used to uncover an inverse gene-for-gene interaction where virulence genes from the pathogen Pyrenophora teres f. maculata target barley susceptibility genes, resulting in disease.

Abstract

Although models have been proposed to broadly explain how plants and pathogens interact and coevolve, each interaction evolves independently, resulting in various scenarios of host manipulation and plant defense. Spot form net blotch is a foliar disease of barley caused by Pyrenophora teres f. maculata. We developed a barley population (Hockett × PI 67381) segregating for resistance to a diverse set of P. teres f. maculata isolates. Quantitative trait locus analysis identified major loci on barley chromosomes (Chr) 2H and 7H associated with resistance/susceptibility. Subsequently, we used avirulent and virulent P. teres f. maculata isolates to develop a pathogen population, identifying two major virulence loci located on Chr1 and Chr2. To further characterize this host–pathogen interaction, progeny from the pathogen population harboring virulence alleles at either the Chr1 or Chr2 locus was phenotyped on the Hockett × PI 67381 population. Progeny harboring only the Chr1 virulence allele lost the barley Chr7H association but maintained the 2H association. Conversely, isolates harboring only the Chr2 virulence allele lost the barley Chr2H association but maintained the 7H association. Hockett × PI 67381 F2 individuals showed susceptible/resistant ratios not significantly different than 15:1 and results from F2 inoculations using the single virulence genotypes were not significantly different from a 3:1 (S:R) ratio, indicating two dominant susceptibility genes. Collectively, this work shows that P. teres f. maculata virulence alleles at the Chr1 and Chr2 loci are targeting the barley 2H and 7H susceptibility alleles in an inverse gene-for-gene manner to facilitate colonization.

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Data availability

All data associated with this study are available in the supplementary data (Online Resource 3) or upon request from the corresponding author.

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Acknowledgements

We would like to thank Danielle Holmes for technical assistance in the lab and greenhouse.

Funding

Financial support was provided by the North Dakota Barley Council, the USDA-NIFA award # 2018–67014-28491 and the National Science Foundation award # 1759030.

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Authors

Contributions

RMS, NAW, and TLF designed the experiments. JDF and RSB generated sequencing data for the barley and P. teres markers, respectively. RMS, NAW, and GKK performed mapping, phenotyping and QTL analysis. RMS and TLF analyzed the data and wrote the manuscript. All authors edited and approved the manuscript.

Corresponding author

Correspondence to Timothy L. Friesen.

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The authors declare that there are no conflicts of interest.

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Communicated by Reem Aboukhaddour.

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Supplementary file2 (XLSX 1053 KB)

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Skiba, R.M., Wyatt, N.A., Kariyawasam, G.K. et al. Host and pathogen genetics reveal an inverse gene-for-gene association in the P. teres f. maculata–barley pathosystem. Theor Appl Genet 135, 3597–3609 (2022). https://doi.org/10.1007/s00122-022-04204-x

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  • DOI: https://doi.org/10.1007/s00122-022-04204-x

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