Hartmann Fanny E, Vonlanthen Tiziana, Singh Nikhil Kumar, McDonald Megan C, Milgate Andrew, Croll Daniel
Ecologie Systematique Evolution, Batiment 360, Université Paris-Saclay, AgroParisTech, CNRS, Orsay, France.
Plant Pathology, Institute of Integrative Biology, ETH Zürich, Zürich, Switzerland.
Mol Ecol. 2021 Nov;30(21):5390-5405. doi: 10.1111/mec.15737. Epub 2020 Dec 12.
Convergent evolution leads to identical phenotypic traits in different species or populations. Convergence can be driven by standing variation allowing selection to favour identical alleles in parallel or the same mutations can arise independently. However, the molecular basis of such convergent adaptation remains often poorly resolved. Pesticide resistance in agricultural ecosystems is a hallmark of convergence in phenotypic traits. Here, we analyse the major fungal pathogen Zymoseptoria tritici causing serious losses on wheat and with fungicide resistance emergence across several continents. We sampled three population pairs each from a different continent spanning periods early and late in the application of fungicides. To identify causal loci for resistance, we combined knowledge from molecular genetics work and performed genome-wide association studies (GWAS) on a global set of isolates. We discovered yet unknown factors in azole resistance including a gene encoding membrane associated functions. We found strong support for the "hotspot" model of resistance evolution with convergent changes in a small set of loci but additional loci showed more population-specific allele frequency changes. Genome-wide scans of selection showed that half of all known resistance loci were overlapping a selective sweep region. Hence, the application of fungicides was one of the major selective agents acting on the pathogen over the past decades. Furthermore, loci identified through GWAS showed the highest overlap with selective sweep regions underlining the importance to map phenotypic trait variation in evolving populations. Our population genomic analyses highlighted that both de novo mutations and gene flow contributed to convergent pesticide adaptation.
趋同进化导致不同物种或种群出现相同的表型特征。趋同现象可能由现存变异驱动，使选择能够平行地青睐相同的等位基因，或者相同的突变能够独立出现。然而，这种趋同适应的分子基础往往仍未得到很好的解析。农业生态系统中的抗药性是表型特征趋同的一个标志。在此，我们分析了主要的真菌病原体小麦叶枯病菌，它在小麦上造成严重损失，并且在几大洲都出现了抗药性。我们从不同大洲分别采集了三对种群样本，涵盖了杀菌剂使用早期和晚期的时间段。为了确定抗药的因果位点，我们结合了分子遗传学研究的知识，并对一组全球分离株进行了全基因组关联研究（GWAS）。我们发现了唑类抗性中尚未知晓的因素，包括一个编码膜相关功能的基因。我们发现有力证据支持抗性进化的“热点”模型，即一小部分位点发生趋同变化，但其他位点显示出更多种群特异性的等位基因频率变化。全基因组选择扫描表明，所有已知抗性位点中有一半与一个选择性清除区域重叠。因此，在过去几十年中，杀菌剂的应用是作用于该病原体的主要选择因素之一。此外，通过GWAS鉴定出的位点与选择性清除区域的重叠度最高，这突出了在不断进化的种群中绘制表型特征变异图谱的重要性。我们的种群基因组分析强调，从头突变和基因流都促成了趋同的农药适应性。
