Cytoplasmic effects (CEs) have been discovered to influence a diverse array of agronomic traits in crops, and understanding the underlying mechanisms can help accelerate breeding programs. Seed oil content (SOC) is of great agricultural, nutritional, and economic importance. However, the genetic basis of CEs on SOC (CE-SOC) remains enigmatic. In this study, we use an optimized approach to sequence the cytoplasmic (plastid and mitochondrial) genomes of allotetraploid oilseed rape (Brassica napus) cultivars, 51218 and 56366, that bear contrasting CE-SOC. By combining comparative genomics and genome-wide transcriptome analysis, we identify mitochondria-encoded orf188 as a potential CE-SOC determinant gene. Functional analyses in the model system Arabidopsis thaliana and rapeseed demonstrated that orf188 governs CE-SOC and could significantly increase SOC, strikingly, through promoting the yield of ATP. Consistent with this finding, transcriptional profiling with microarray and RNA sequencing revealed that orf188 affects transcriptional reprogramming of mitochondrial energy metabolism to facilitate ATP production. Intriguingly, orf188 is a previously uncharacterized chimeric gene, and the presence of this genetic novelty endows rapeseed with positive CE-SOC. Our results shed light on the molecular basis of CEs on a key quantitative trait in polyploid crops and enrich the theory of maternal control of oil content, providing new scientific guidance for breeding high-oil rapeseed germplasms.

已经发现细胞质效应（CEs）会影响农作物的多种农艺性状，并且了解其潜在机制可以帮助加快育种程序。种子油含量（SOC）在农业，营养和经济方面均具有重要意义。然而，基于SOC的CE的遗传基础（CE-SOC）仍然是个谜。在这项研究中，我们使用一种优化的方法来对异源四倍体油菜（甘蓝型油菜）品种51218和56366的细胞质（质体和线粒体）基因组进行测序，它们具有相反的CE-SOC。通过结合比较基因组学和全基因组转录组分析，我们确定线粒体编码的orf188作为潜在的CE-SOC决定基因。模型系统拟南芥中的功能分析油菜籽证明orf188支配CE-SOC，并通过提高ATP的产量显着提高SOC。与此发现一致的是，利用微阵列和RNA测序进行转录谱分析表明，orf188影响线粒体能量代谢的转录重编程，从而促进ATP的产生。有趣的是，orf188是一个以前未鉴定的嵌合基因，而这种遗传新奇的存在赋予了菜籽油菜籽CE-SOC阳性。我们的研究结果揭示了多倍体农作物中CEs关键定量性状的分子基础，丰富了母体控制油含量的理论，为育种高油菜籽种质提供了新的科学指导。