To identify cytoplasmic male sterility (CMS)-associated genes in tomato, we determined the genome sequences of mitochondria and chloroplasts in three CMS tomato lines derived from independent asymmetric cell fusions, their nuclear and cytoplasmic donors, and male fertile weedy cultivated tomato and wild relatives. The structures of the CMS mitochondrial genomes were highly divergent from those of the nuclear and cytoplasmic donors, and genes of the donors were mixed up in these genomes. On the other hand, the structures of CMS chloroplast genomes were moderately conserved across the donors, but CMS chloroplast genes were unexpectedly likely derived from the nuclear donors. Comparative analysis of the structures and contents of organelle genes and transcriptome analysis identified three genes that were uniquely present in the CMS lines, but not in the donor or fertile lines. RNA-sequencing analysis indicated that these three genes transcriptionally expressed in anther, and identified different RNA editing levels in one gene, orf265, that was partially similar to ATP synthase subunit 8, between fertile and sterile lines. The orf265 was a highly potential candidate for CMS-associated gene. This study suggests that organelle reorganization mechanisms after cell fusion events differ between mitochondria and chloroplasts, and provides insight into the development of new F1 hybrid breeding programs employing the CMS system in tomato.

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细胞器基因组组装揭示了番茄中的动态基因组重组和细胞质雄性不育相关基因

为了鉴定番茄中的细胞质雄性不育 (CMS) 相关基因，我们确定了三个 CMS 番茄系中线粒体和叶绿体的基因组序列，这些番茄系来自独立的不对称细胞融合、它们的核和细胞质供体，以及雄性可育杂草栽培番茄和野生近缘种. CMS线粒体基因组的结构与核和细胞质供体的结构高度不同，供体的基因在这些基因组中混杂在一起。另一方面，CMS叶绿体基因组的结构在供体中适度保守，但CMS叶绿体基因出人意料地可能来自核供体。细胞器基因的结构和内容的比较分析和转录组分析确定了 CMS 系中唯一存在的三个基因，但不在供体或可育系中。RNA测序分析表明这三个基因在花药中转录表达，并在一个基因中鉴定出不同的RNA编辑水平，orf265, 这部分类似于ATP合酶亚基8，在可育系和不育系之间。这orf265是CMS相关基因的高度潜在候选者。该研究表明，细胞融合事件后的细胞器重组机制在线粒体和叶绿体之间存在差异，并为在番茄中使用 CMS 系统开发新的 F1 杂交育种计划提供了见解。