Department of Biologia Evoluzionistica Sperimentale, University of Bologna, Bologna, Italy.
PLoS One. 2011;6(11):e28194. doi: 10.1371/journal.pone.0028194. Epub 2011 Nov 29.
Doubly Uniparental Inheritance (DUI) of mitochondria occurs when both mothers and fathers are capable of transmitting mitochondria to their offspring, in contrast to the typical Strictly Maternal Inheritance (SMI). DUI was found in some bivalve molluscs, in which two mitochondrial genomes are inherited, one through eggs, the other through sperm. During male embryo development, spermatozoon mitochondria aggregate in proximity of the first cleavage furrow and end up in the primordial germ cells, while they are dispersed in female embryos.
METHODOLOGY/PRINCIPAL FINDINGS: We used MitoTracker, microtubule staining and transmission electron microscopy to examine the mechanisms of this unusual distribution of sperm mitochondria in the DUI species Ruditapes philippinarum. Our results suggest that in male embryos the midbody deriving from the mitotic spindle of the first division concurs in positioning the aggregate of sperm mitochondria. Furthermore, an immunocytochemical analysis showed that the germ line determinant Vasa segregates close to the first cleavage furrow.
CONCLUSIONS/SIGNIFICANCE: In DUI male embryos, spermatozoon mitochondria aggregate in a stable area on the animal-vegetal axis: in organisms with spiral segmentation this zone is not involved in cleavage, so the aggregation is maintained. Moreover, sperm mitochondria reach the same embryonic area in which also germ plasm is transferred. In 2-blastomere embryos, the segregation of sperm mitochondria in the same region with Vasa suggests their contribution in male germ line formation. In DUI male embryos, M-type mitochondria must be recognized by egg factors to be actively transferred in the germ line, where they become dominant replacing the Balbiani body mitochondria. The typical features of germ line assembly point to a common biological mechanism shared by DUI and SMI organisms. Although the molecular dynamics of the segregation of sperm mitochondria in DUI species are unknown, they could be a variation of the mechanism regulating the mitochondrial bottleneck in all metazoans.
与典型的严格母系遗传(SMI)相反,当母亲和父亲都能够将线粒体传递给后代时,就会发生双倍单亲遗传(DUI)。在一些双壳贝类中发现了 DUI,其中两个线粒体基因组通过卵子和精子遗传。在雄性胚胎发育过程中,精子线粒体聚集在第一次卵裂沟附近,最终进入原始生殖细胞,而在雌性胚胎中则分散存在。
方法/主要发现:我们使用 MitoTracker、微管染色和透射电子显微镜检查了 DUI 物种菲律宾蛤仔中这种异常分布的精子线粒体的机制。我们的结果表明,在雄性胚胎中,来自第一次分裂的有丝分裂纺锤体的中间体有助于定位精子线粒体的聚集。此外,免疫细胞化学分析表明,生殖线决定因子 Vasa 靠近第一次卵裂沟分离。
结论/意义:在 DUI 雄性胚胎中,精子线粒体在动物-植物轴上的一个稳定区域聚集:在具有螺旋分割的生物体中,这个区域不参与分裂,因此聚集得以维持。此外,精子线粒体到达与生殖质转移相同的胚胎区域。在 2-胚胎卵中,精子线粒体与 Vasa 聚集在同一区域,表明它们对雄性生殖系形成的贡献。在 DUI 雄性胚胎中,M 型线粒体必须被卵子因子识别,才能主动转移到生殖系中,在那里它们取代 Balbiani 体线粒体成为优势。生殖系组装的典型特征表明 DUI 和 SMI 生物具有共同的生物学机制。尽管 DUI 物种中精子线粒体分离的分子动力学尚不清楚,但它们可能是调节所有后生动物中线粒体瓶颈的机制的一种变体。