Comparative Genomics of the Sigatoka Disease Complex on Banana Suggests a Link between Parallel Evolutionary Changes in <i>Pseudocercospora fijiensis</i> and <i>Pseudocercospora eumusae</i> and Increased Virulence on the Banana Host

The Sigatoka disease complex, caused by the closely-related Dothideomycete fungi Pseudocercospora musae (yellow sigatoka), Pseudocercospora eumusae (eumusae leaf spot), and Pseudocercospora fijiensis (black sigatoka), is currently the most devastating disease on banana worldwide. The three species emerged on bananas from a recent common ancestor and show clear differences in virulence, with P. eumusae and P. fijiensis considered the most aggressive. In order to understand the genomic modifications associated with shifts in the species virulence spectra after speciation, and to identify their pathogenic core that can be exploited in disease management programs, we have sequenced and analyzed the genomes of P. eumusae and P. musae and compared them with the available genome sequence of P. fijiensis. Comparative analysis of genome architectures revealed significant differences in genome size, mainly due to different rates of LTR retrotransposon proliferation. Still, gene counts remained relatively equal and in the range of other Dothideomycetes. Phylogenetic reconstruction based on a set of 46 conserved single-copy genes strongly supported an earlier evolutionary radiation of P. fijiensis from P. musae and P. eumusae. However, pairwise analyses of gene content indicated that the more virulent P. eumusae and P. fijiensis share complementary patterns of expansions and contractions in core gene families related to metabolism and enzymatic degradation of plant cell walls, suggesting that the evolution of virulence in these two pathogens has, to some extent, been facilitated by convergent changes in metabolic pathways associated with nutrient acquisition and assimilation. In spite of their common ancestry and shared host-specificity, the three species retain fairly dissimilar repertoires of effector proteins, suggesting that they likely evolved different strategies for manipulating the host immune system. Finally, 234 gene families, including seven putative effectors, were exclusively present in the three Sigatoka species, and could thus be related to adaptation to the banana host.由近缘的座囊菌纲（Dothideomycetes）真菌香蕉生假尾孢（Pseudocercospora musae，引发黄Sigatoka病）、厄尔马斯假尾孢（Pseudocercospora eumusae，引发厄尔马斯叶斑病）以及斐济假尾孢（Pseudocercospora fijiensis，引发黑Sigatoka病）所导致的Sigatoka病复合体，是目前全球范围内为害最严重的香蕉病害。这三个菌种均起源于近期的共同祖先，且致病力存在显著差异，其中厄尔马斯假尾孢与斐济假尾孢被认为是致病力最强的两个菌种。为解析物种形成后致病力谱分化相关的基因组变异，并挖掘可应用于病害防控策略的核心致病因子，本研究对厄尔马斯假尾孢与香蕉生假尾孢的基因组进行测序与分析，并与已公布的斐济假尾孢基因组序列开展比较分析。基因组结构比较分析显示，三个菌种的基因组大小存在显著差异，这主要源于长末端重复序列反转录转座子（LTR retrotransposon）的增殖速率不同；但基因数量基本保持一致，且与其他座囊菌纲真菌的基因数量处于同一区间。基于46个保守单拷贝基因构建的系统发育树，强烈支持斐济假尾孢更早从香蕉生假尾孢与厄尔马斯假尾孢的共同祖先中分化出来的演化关系。然而基因含量的成对比较分析显示，致病力更强的厄尔马斯假尾孢与斐济假尾孢在与代谢及植物细胞壁酶解相关的核心基因家族中，呈现出互补的扩张与收缩模式，这表明这两种病原菌的致病力演化在一定程度上得益于与营养获取和同化相关的代谢通路的趋同变异。尽管这三个菌种拥有共同的祖先且均为香蕉专化性病原菌，但其效应蛋白组存在显著差异，这暗示它们演化出了不同的宿主免疫系统调控策略。最后，共有234个基因家族（包含7个假定效应蛋白）仅存在于三个Sigatoka病相关假尾孢菌种中，这提示这些基因家族可能与病原菌对香蕉寄主的适应性演化相关。