Smith Chase H, Mejia-Trujillo Raquel, Breton Sophie, Pinto Brendan J, Kirkpatrick Mark, Havird Justin C
Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA.
Department of Biological Sciences, University of Montreal, Montreal, Canada.
bioRxiv. 2023 Jul 7:2023.07.05.547839. doi: 10.1101/2023.07.05.547839.
Genetic elements encoded in nuclear DNA determine the sex of an individual in many animals. In bivalves, however, mitochondrial DNA (mtDNA) has been hypothesized to contribute to sex determination in lineages that possess doubly uniparental inheritance (DUI). In these cases, females transmit a female mtDNA (F mtDNA) to all offspring, while male mtDNA (M mtDNA) is transmitted only from fathers to sons. Because M mtDNA is inherited in the same way as Y chromosomes, it has been hypothesized that mtDNA may be responsible for sex determination. However, the role of mitochondrial and nuclear genes in sex determination has yet to be validated in DUI bivalves. In this study, we used DNA, RNA, and mitochondrial short non-coding RNA (sncRNA) sequencing to explore the role of mitochondrial and nuclear elements in the sexual development pathway of the freshwater mussel (Bivalvia: Unionida). We found that the M mtDNA shed a sncRNA partially within a male-specific mitochondrial gene that targeted pathways hypothesized to be involved in female development and mitophagy. RNA-seq confirmed the gene target was significantly upregulated in females, supporting a direct role of mitochondrial sncRNAs in gene silencing. These findings support the hypothesis that M mtDNA inhibits female development. Genome-wide patterns of genetic differentiation and heterozygosity did not support a nuclear sex determining region, although we cannot reject that nuclear factors are involved with sex determination. Our results provide further evidence that mitochondrial loci contribute to diverse, non-respiratory functions and provide a first glimpse into an unorthodox sex determining system.
核DNA中编码的遗传元件决定了许多动物个体的性别。然而，在双壳贝类中，线粒体DNA（mtDNA）被认为在具有双单亲遗传（DUI）的谱系中对性别决定有贡献。在这些情况下，雌性将雌性mtDNA（F mtDNA）传递给所有后代，而雄性mtDNA（M mtDNA）仅从父亲传递给儿子。由于M mtDNA与Y染色体的遗传方式相同，因此有人推测mtDNA可能负责性别决定。然而，线粒体和核基因在性别决定中的作用尚未在具有DUI的双壳贝类中得到验证。在本研究中，我们使用DNA、RNA和线粒体短非编码RNA（sncRNA）测序来探索线粒体和核元件在淡水贻贝（双壳纲：蚌目）性发育途径中的作用。我们发现，M mtDNA在一个雄性特异性线粒体基因内部分释放了一种sncRNA，该基因靶向假设参与雌性发育和线粒体自噬的途径。RNA测序证实该基因靶点在雌性中显著上调，支持线粒体sncRNA在基因沉默中的直接作用。这些发现支持了M mtDNA抑制雌性发育的假设。全基因组的遗传分化和杂合性模式不支持存在核性别决定区域，尽管我们不能排除核因子参与性别决定的可能性。我们的结果进一步证明线粒体基因座有助于多种非呼吸功能，并首次揭示了一种非传统的性别决定系统。
