Multiple Interkingdom Horizontal Gene Transfers in <i>Pyrenophora</i> and Closely Related Species and Their Contributions to Phytopathogenic Lifestyles

Many studies have reported horizontal gene transfer (HGT) events from eukaryotes, especially fungi. However, only a few investigations summarized multiple interkingdom HGTs involving important phytopathogenic species of Pyrenophora and few have investigated the genetic contributions of HGTs to fungi. We investigated HGT events in P. teres and P. tritici-repentis and discovered that both species harbored 14 HGT genes derived from bacteria and plants, including 12 HGT genes that occurred in both species. One gene coding a leucine-rich repeat protein was present in both species of Pyrenophora and it may have been transferred from a host plant. The transfer of genes from a host plant to pathogenic fungi has been reported rarely and we discovered the first evidence for this transfer in phytopathogenic Pyrenophora. Two HGTs in Pyrenophora underwent subsequent duplications. Some HGT genes had homologs in a few other fungi, indicating relatively ancient transfer events. Functional analyses indicated that half of the HGT genes encoded extracellular proteins and these may have facilitated the infection of plants by Pyrenophora via interference with plant defense-response and the degradation of plant cell walls. Some other HGT genes appeared to participate in carbohydrate metabolism. Together, these functions implied that HGTs may have led to highly efficient mechanisms of infection as well as the utilization of host carbohydrates. Evolutionary analyses indicated that HGT genes experienced amelioration, purifying selection, and accelerated evolution. These appeared to constitute adaptations to the background genome of the recipient. The discovery of multiple interkingdom HGTs in Pyrenophora, their significance to infection, and their adaptive evolution, provided valuable insights into the evolutionary significance of interkingdom HGTs from multiple donors.已有多项研究报道了源自真核生物（尤其是真菌）的水平基因转移（horizontal gene transfer, HGT）事件。然而，目前仅有少数研究总结了涉及核腔菌属（Pyrenophora）重要植物病原物种的跨域水平基因转移事件，且鲜有研究探讨水平基因转移对真菌的遗传贡献。本研究针对大麦网斑核腔菌（P. teres）与小麦黄斑核腔菌（P. tritici-repentis）的水平基因转移事件展开分析，发现这两个物种均携带14个源自细菌与植物的水平基因转移基因，其中12个基因在两个物种中均存在。其中一个编码富亮氨酸重复蛋白的基因在两个核腔菌属物种中均存在，推测其源自宿主植物的水平转移。宿主植物向病原真菌的基因转移事件此前鲜有报道，本研究首次在植物病原核腔菌属中发现了此类转移的证据。核腔菌属中的两个水平基因转移基因后续发生了复制事件。部分水平基因转移基因在少数其他真菌中存在同源序列，提示这些转移事件发生年代相对久远。功能分析结果显示，半数水平基因转移基因编码胞外蛋白，此类蛋白可能通过干扰植物防御反应、降解植物细胞壁，助力核腔菌属真菌侵染宿主植物。另有部分水平基因转移基因似乎参与了碳水化合物代谢过程。综合上述功能推测，水平基因转移可能帮助核腔菌属真菌演化出高效的侵染机制，并提升其对宿主碳水化合物的利用能力。进化分析结果显示，水平基因转移基因经历了适应性优化、纯化选择以及加速进化过程。这些进化特征似乎是对受体真菌背景基因组的适应性演化。核腔菌属中跨域水平基因转移事件的发现、其对侵染过程的重要意义，以及它们的适应性演化特征，为解析多供体来源跨域水平基因转移的进化意义提供了重要见解。