Table_1_Mitochondrial Genomics of Six Cacao Pathogens From the Basidiomycete Family Marasmiaceae.XLSX

Thread blight disease has recently been described as an emerging disease on cacao (Theobroma cacao) in Ghana. In Ghana, thread blight disease is caused by multiple species of the Marasmiaceae family: Marasmius tenuissimus, M. crinis-equi, M. palmivorus, and Marasmiellus scandens. Interestingly, two additional members of the Marasmiaceae; Moniliophthora roreri (frosty pod rot) and Moniliophthora perniciosa (witches’ broom disease), are major pathogens of cacao in the Western hemisphere. It is important to accurately characterize the genetic relationships among these economically important species in support of their disease management. We used data from Illumina NGS-based genome sequencing efforts to study the mitochondrial genomes (mitogenomes) of the four cacao thread blight associated pathogens from Ghana and compared them with published mitogenomes of Mon. roreri and Mon. perniciosa. There is a remarkable interspecies variation in mitogenome size within the six cacao-associated Marasmiaceae species, ranging from 43,121 to 109,103 bp. The differences in genome lengths are primarily due to the number and lengths of introns, differences in intergenic space, and differences in the size and numbers of unidentified ORFs (uORF). Among seven M. tenuissimus mitogenomes sequenced, there is variation in size and sequence pointing to divergent evolution patterns within the species. The intronic regions show a high degree of sequence variation compared to the conserved sequences of the 14 core genes. The intronic ORFs identified, regardless of species, encode GIY-YIG or LAGLIDADG domain-containing homing endonuclease genes. Phylogenetic relationships using the 14 core proteins largely mimic the phylogenetic relationships observed in gene order patterns, grouping M. tenuissimus with M. crinis-equi, and M. palmivorus with Mon. roreri and Mon. perniciosa, leaving Mar. scandens as an outlier. The results from this study provide evidence of independent expansion/contraction events and sequence diversification in each species and establish a foundation for further exploration of the evolutionary trajectory of the fungi in Marasmiaceae family.

近日，加纳的可可树（Theobroma cacao）上被报道出现一种新兴病害——线疫病（Thread blight disease）。在加纳，该线疫病由小皮伞科（Marasmiaceae）的多个物种引起：细小小皮伞（Marasmius tenuissimus）、马毛小皮伞（M. crinis-equi）、棕榈小皮伞（M. palmivorus）以及攀援小奥德蘑（Marasmiellus scandens）。值得注意的是，小皮伞科另外两个成员——可可霜霉荚腐病病原Moniliophthora roreri（Mon. roreri，frosty pod rot）和可可丛枝病病原Moniliophthora perniciosa（Mon. perniciosa，witches’ broom disease），是西半球可可的主要病原菌。准确解析这些具有经济重要性的物种间的遗传关系，对其病害防控具有重要支撑意义。本研究利用基于Illumina下一代测序（Next-Generation Sequencing, NGS）的基因组测序数据，对加纳4种与可可线疫病相关的病原菌的线粒体基因组（mitochondrial genomes, mitogenomes）进行了研究，并将其与已发表的Mon. roreri和Mon. perniciosa的线粒体基因组进行了比较分析。6种与可可相关的小皮伞科物种的线粒体基因组大小存在显著的种间差异，范围为43121 bp至109103 bp。基因组长度差异主要源于内含子的数量与长度、基因间隔区的差异，以及未鉴定开放阅读框（unidentified ORFs, uORF）的大小和数量差异。在已测序的7个细小小皮伞线粒体基因组中，其大小和序列均存在变异，表明该物种内部存在趋异演化模式。与14个核心基因的保守序列相比，内含子区域表现出高度的序列变异。所鉴定出的内含子开放阅读框，无论所属物种如何，均编码含GIY-YIG结构域（GIY-YIG domain）或LAGLIDADG结构域（LAGLIDADG domain）的归巢内切酶基因。基于14个核心蛋白构建的系统发育关系，与基因顺序模式所呈现的系统发育关系大体一致：细小小皮伞与马毛小皮伞聚为一支，棕榈小皮伞与Mon. roreri、Mon. perniciosa聚为一支，而攀援小奥德蘑（Mar. scandens）则作为独立外类群。本研究结果为每个物种独立发生的基因组扩张/收缩事件及序列多样化提供了证据，并为进一步探究小皮伞科真菌的演化轨迹奠定了基础。