Pyrenophora tritici-repentis (tan spot) is a destructive foliar pathogen of wheat with global impact. This ascomycete fungus possesses a highly plastic open pangenome shaped by the gain and loss of effector genes. This study investigated the allelic variations in the chlorosis-encoding gene ToxB across 422 isolates representing all identified pathotypes and worldwide origins. To gain better insights into ToxB evolution, we examined its presence and variability in other Pyrenophora spp. A ToxB haplotype network was constructed, revealing the evolutionary relationships of this gene (20 haplotypes) across four Pyrenophora species. Notably, toxb, the homolog of ToxB, was detected for the first time in the barley pathogen Pyrenophora teres. The ToxB/toxb genes display evidence of selection that is characterized by loss of function, duplication, and diverse mutations. Within the ToxB/toxb open reading frame, 72 mutations were identified, including 14 synonymous, 55 nonsynonymous, and 3 indel mutations. Remarkably, a, ∼5.6-kb Copia-like retrotransposon, named Copia-1_Ptr, was found inserted in the toxb gene of a race 3 isolate. This insert disrupted the ToxB gene's function, a first case of effector gene disruption by a transposable element in P. tritici-repentis. Additionally, a microsatellite with 25 nucleotide repeats (0 to 10) in the upstream region of ToxB suggested a potential mechanism influencing ToxB expression and regulation. Exploring ToxB-like protein distribution in other ascomycetes revealed the presence of ToxB-like proteins in 19 additional species, including the Leotiomycetes class for the first time. The presence/absence pattern of ToxB-like proteins defied species relatedness compared with a phylogenetic tree, suggesting a past horizontal gene transfer event during the evolution of the ToxB gene.

Copyright © 2024 His Majesty the King in Right of Canada, as represented by the Minister of Agriculture and Agri-Food. This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

小麦白斑病（棕斑病）是一种具有全球影响的小麦叶面病原菌。这种子囊菌拥有高度可塑性的开放全基因组，由效应基因的获得和丢失形成。这项研究调查了422 个代表所有已识别致病型和全球起源的分离株中缺绿病编码基因ToxB 的等位基因变异。为了更好地了解ToxB 的进化，我们研究了它在其他核腔菌属中的存在和变异性。构建了ToxB单倍型网络，揭示了该基因（20 个单倍型）在四种核腔菌属物种中的进化关系。值得注意的是，Toxb （ ToxB的同源物）首次在大麦病原体圆核腔菌中检测到。ToxB / toxb基因显示出选择的证据，其特征是功能丧失、重复和多样化突变。在ToxB / toxb开放阅读框中，鉴定出72个突变，包括14个同义突变、55个非同义突变和3个插入缺失突变。值得注意的是，一个~5.6-kb Copia 样逆转录转座子，名为 Copia-1_Ptr，被发现插入到了3 号种族分离株的toxb基因中。该插入破坏了ToxB基因的功能，这是白小麦中转座元件破坏效应基因的第一例。此外， ToxB上游区域具有 25 个核苷酸重复（0 至 10）的微卫星表明存在影响ToxB表达和调节的潜在机制。探索 ToxB 样蛋白在其他子囊菌中的分布，首次揭示了 ToxB 样蛋白在另外 19 个物种中的存在，其中包括 Leotiomycetes 类。与系统发育树相比，ToxB 样蛋白的存在/不存在模式违背了物种相关性，这表明ToxB基因进化过程中过去存在水平基因转移事件。

版权所有 © 2024 加拿大国王陛下，由农业和农业食品部长代表。这是一篇根据 CC BY-NC-ND 4.0 国际许可证分发的开放获取文章。