Department of Agricultural Biology, Colorado State University, Fort Collins, Colorado, USA.
U.S. Department of Energy Joint Genome Institute, Berkeley, California, USA.
Genome Biol Evol. 2021 Feb 3;13(2). doi: 10.1093/gbe/evaa267.
The genus Claviceps has been known for centuries as an economically important fungal genus for pharmacology and agricultural research. Only recently have researchers begun to unravel the evolutionary history of the genus, with origins in South America and classification of four distinct sections through ecological, morphological, and metabolic features (Claviceps sects. Citrinae, Paspalorum, Pusillae, and Claviceps). The first three sections are additionally characterized by narrow host range, whereas section Claviceps is considered evolutionarily more successful and adaptable as it has the largest host range and biogeographical distribution. However, the reasons for this success and adaptability remain unclear. Our study elucidates factors influencing adaptability by sequencing and annotating 50 Claviceps genomes, representing 21 species, for a comprehensive comparison of genome architecture and plasticity in relation to host range potential. Our results show the trajectory from specialized genomes (sects. Citrinae and Paspalorum) toward adaptive genomes (sects. Pusillae and Claviceps) through colocalization of transposable elements around predicted effectors and a putative loss of repeat-induced point mutation resulting in unconstrained tandem gene duplication coinciding with increased host range potential and speciation. Alterations of genomic architecture and plasticity can substantially influence and shape the evolutionary trajectory of fungal pathogens and their adaptability. Furthermore, our study provides a large increase in available genomic resources to propel future studies of Claviceps in pharmacology and agricultural research, as well as, research into deeper understanding of the evolution of adaptable plant pathogens.
百年来，麦角菌属一直是药理学和农业研究中具有重要经济价值的真菌属。直到最近，研究人员才开始揭示该属的进化历史，其起源于南美洲，并通过生态、形态和代谢特征将其分为四个不同的节（麦角菌属 Claviceps 节 Citrinae、Paspalorum、Pusillae 和 Claviceps）。前三个节还具有狭窄的宿主范围，而 Claviceps 节被认为在进化上更成功和适应性更强，因为它具有最大的宿主范围和生物地理分布。然而，这种成功和适应性的原因尚不清楚。我们的研究通过对代表 21 个种的 50 个麦角菌基因组进行测序和注释，阐明了影响适应性的因素，全面比较了与宿主范围潜力相关的基因组结构和可塑性。我们的研究结果表明，从专门的基因组（Citrinae 和 Paspalorum 节）到适应性基因组（Pusillae 和 Claviceps 节）的轨迹是通过预测效应子周围转座元件的共定位以及重复诱导点突变的潜在丧失而实现的，这导致了不受约束的串联基因重复，同时伴随着宿主范围潜力和物种形成的增加。基因组结构和可塑性的改变可以极大地影响和塑造真菌病原体的进化轨迹及其适应性。此外，我们的研究提供了大量可用的基因组资源，以推动未来在药理学和农业研究中对麦角菌的研究，以及更深入地研究适应性植物病原体的进化。
