Emerging fungal pathogens are a threat to forest and agroecosystems, as well as animal and human health. How pathogens evolve from nonpathogenic ancestors is still poorly understood, making the prediction of future outbreaks challenging. Most pathogens have evolved lifestyle adaptations, which were enabled by specific changes in the gene content of the species. Hence, understanding transitions in the functions encoded by genomes gives valuable insight into the evolution of pathogenicity. Here, we studied lifestyle evolution in the genus Cryphonectria, including the prominent invasive pathogen Cryphonectria parasitica, the causal agent of chestnut blight on Castanea species. We assembled and compared the genomes of pathogenic and putatively nonpathogenic Cryphonectria species, as well as sister group pathogens in the family Cryphonectriaceae (Diaporthales, Ascomycetes), to investigate the evolution of genome size and gene content. We found a striking loss of genes associated with carbohydrate metabolism (CAZymes) in C. parasitica compared to other Cryphonectriaceae. Despite substantial CAZyme gene loss, experimental data suggest that C. parasitica has retained wood colonization abilities shared with other Cryphonectria species. Putative effectors substantially varied in number, cysteine content, and protein length among species. In contrast, secondary metabolite gene clusters show a high degree of conservation within the genus. Overall, our results underpin the recent lifestyle transition of C. parasitica toward a more pathogenic lifestyle. Our findings suggest that a CAZyme loss may have promoted pathogenicity of C. parasitica on Castanea species. Analyzing gene complements underlying key nutrition modes can facilitate the detection of species with the potential to emerge as pathogens.

中文翻译：

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在 Cryphonectria 属侵袭性真菌病原体起源处生活方式转变的比较基因组学分析

新出现的真菌病原体对森林和农业生态系统以及动物和人类健康构成威胁。病原体如何从非致病性祖先进化至今仍知之甚少，这使得对未来爆发的预测具有挑战性。大多数病原体已经进化出生活方式适应，这是通过物种基因含量的特定变化实现的。因此，了解基因组编码的功能转变为了解致病性进化提供了宝贵的见解。在这里，我们研究了Cryphonectria属的生活方式演变，包括突出的入侵病原体Cryphonectria parasitica，它是栗属物种板栗枯萎病的病原体。我们组装并比较了致病性和假定非致病性的基因组Cryphonectria物种，以及 Cryphonectriaceae (Diaporthales, Ascomycetes) 中的姐妹群病原体，以研究基因组大小和基因含量的进化。我们发现与其他 Cryphonectriaceae 相比，C. parasitica中与碳水化合物代谢 (CAZymes) 相关的基因显着丢失。尽管 CAZyme 基因大量丢失，但实验数据表明C. parasitica保留了与其他Cryphonectria物种共享的木材定植能力。假定的效应子在数量、半胱氨酸含量和蛋白质长度方面在物种之间有很大差异。相比之下，次生代谢物基因簇在属内表现出高度的保守性。总的来说，我们的结果支持了最近的生活方式转变C. parasitica走向更具致病性的生活方式。我们的研究结果表明，CAZyme 丢失可能促进了C. parasitica对栗属物种的致病性。分析潜在的关键营养模式的基因补充可以促进检测有可能成为病原体的物种。