Sampaio Ana Margarida, Tralamazza Sabina Moser, Mohamadi Faharidine, De Oliveira Yannick, Enjalbert Jérôme, Saintenac Cyrille, Croll Daniel
Laboratory of Evolutionary Genetics, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.
Arvalis - Institut du Végétal, Station expérimentale, Boigneville, France.
PLoS Pathog. 2025 Mar 31;21(3):e1012983. doi: 10.1371/journal.ppat.1012983. eCollection 2025 Mar.
Interactions between plant pathogens and their hosts are highly dynamic and mainly driven by pathogen effectors and plant receptors. Host-pathogen co-evolution can cause rapid diversification or loss of pathogen genes encoding host-exposed proteins. The molecular mechanisms that underpin such sequence dynamics remains poorly investigated at the scale of entire pathogen species. Here, we focus on AvrStb6, a major effector of the global wheat pathogen Zymoseptoria tritici, evolving in response to the cognate receptor Stb6, a resistance widely deployed in wheat. We comprehensively captured effector gene evolution by analyzing a global thousand-genome panel using reference-free sequence analyses. We found that AvrStb6 has diversified into 59 protein isoforms with a strong association to the pathogen spreading to new continents. Across Europe, we found the strongest differentiation of the effector consistent with high rates of Stb6 deployment. The AvrStb6 locus showed also a remarkable diversification in transposable element content with specific expansion patterns across the globe. We detected AvrStb6 gene losses and evidence for transposable element-mediated disruptions. We used virulence datasets of genome-wide association mapping studies to predict virulence changes across the global panel. Genomic predictions suggested marked increases in virulence on Stb6 cultivars concomitant with the spread of the pathogen to Europe and the subsequent spread to further continents. Finally, we genotyped French bread wheat cultivars for Stb6 and monitored resistant cultivar deployment concomitant with AvrStb6 evolution. Taken together, our data provides a comprehensive view of how a rapidly diversifying effector locus can undergo large-scale sequence changes concomitant with gains in virulence on resistant cultivars. The analyses highlight also the need for large-scale pathogen sequencing panels to assess the durability of resistance genes and improve the sustainability of deployment strategies.
植物病原体与其宿主之间的相互作用高度动态，主要由病原体效应子和植物受体驱动。宿主 - 病原体的共同进化可导致编码宿主暴露蛋白的病原体基因快速多样化或丢失。在整个病原体物种层面，支撑这种序列动态变化的分子机制仍未得到充分研究。在此，我们聚焦于AvrStb6，它是全球小麦病原体小麦黄斑叶枯病菌（Zymoseptoria tritici）的主要效应子，其进化是为了应对同源受体Stb6，Stb6是一种在小麦中广泛应用的抗性基因。我们通过使用无参考序列分析方法分析全球千基因组数据集，全面捕捉了效应子基因的进化情况。我们发现AvrStb6已多样化为59种蛋白质异构体，这与病原体传播到新大陆密切相关。在欧洲各地，我们发现效应子的分化最为强烈，这与Stb6的高应用率一致。AvrStb6基因座在转座子含量方面也呈现出显著的多样化，在全球具有特定的扩增模式。我们检测到了AvrStb6基因的丢失以及转座子介导的破坏证据。我们利用全基因组关联图谱研究的毒力数据集来预测全球样本中的毒力变化。基因组预测表明，随着病原体传播到欧洲并随后扩散到其他大陆，对携带Stb6基因的品种的毒力显著增加。最后，我们对法国面包小麦品种进行了Stb6基因分型，并监测了抗性品种的应用情况以及AvrStb6的进化。综上所述，我们的数据全面展示了一个快速多样化的效应子基因座如何伴随对抗性品种毒力的增加而经历大规模的序列变化。这些分析还凸显了需要大规模病原体测序数据集来评估抗性基因的持久性并改善应用策略的可持续性。
