Population genomic analyses and demography inference show recent emergence and dispersal of barley pathogen coinciding with crop domestication and cultivation history

Authors: TALIADOROS, DEMETRIS - Max Planck Institute For Evolutionary Biology; FEURTEY, ALICE - Max Planck Institute For Evolutionary Biology; Wyatt, Nathan; GLADIEUX, PIERRE - University Of Montpellier; Friesen, Timothy; STUKENBROCK, EVA - Max Planck Institute For Evolutionary Biology

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/15/2024
Publication Date: 1/29/2024
Citation: Taliadoros, D., Feurtey, A., Wyatt, N.A., Gladieux, P., Friesen, T.L., Stukenbrock, E. 2024. Population genomic analyses and demography inference show recent emergence and dispersal of barley pathogen coinciding with crop domestication and cultivation history. PLoS Genetics. https://doi.org/10.1371/journal.pgen.1010884.
DOI: https://doi.org/10.1371/journal.pgen.1010884

Interpretive Summary: Fungal pathogens regularly cause disease epidemics on food crops globally. Understanding the evolutionary origin of the pathogens causing these epidemics is critical for scientists, breeders, and growers to develop and implement control strategies to reduce yield and quality losses. Here we have used a global collection of Pyrenophora teres f. teres (causal agent of net form net blotch of barley) in conjunction with machine learning to reconstruct the evolutionary history of this economically important pathogen of barley. This work shows that P. teres f. teres has adapted to local environments likely including local weather conditions and resistance in locally planted cultivars. This information is critical to extension pathologists and agronomists making recommendations for control strategies, as well as breeders that are actively introgressing resistance into locally planted cultivars.

Technical Abstract: Fungal pathogens cause devastating disease in crops. Understanding the evolutionary origin of pathogens is essential to the prediction future disease emergence and the potential of pathogens to disperse. The fungus Pyrenophora teres f. teres causes nNet form net blotch (NFNB), an severeeconomically significant disease of barley. In this study, we have used 104 P. teres f. teres genomes from four continents to explore the history of P. teres f. teres. Using a population genomic approach we explored population structure of the fungal pathogen and characterised patterns of genetic variation among populations. We further applied a Multiple Sequentially Markovian Coalescent approach and a machine learning method to reconstruct the population history of P. teres f. teres. Hereby we demonstrate that the inferred demographic history of the pathogen correlates with the history of its host, barley highlighting the importance of human migration and trading in the dispersal of the pathogen. Exploring signatures of selection along the haploid genome, we identify several population-specific selective sweeps, rather than sweeps shared across all populations. This may reflect rapid adaptation to local hosts and environmental conditions of P. teres f. teres. In support of this hypothesis, we identify selective sweeps colocalizing with genomic regions enriched in putative virulence genes encoding virulence traits, and loci previously identified as determinants of virulence specificities by quantitative trait locus analyses.