Department of Genetics, Stanford University School of Medicine, Stanford, CA.
Department of Animal Sciences, Wageningen University, Wageningen, The Netherlands.
Mol Biol Evol. 2020 Sep 1;37(9):2679-2690. doi: 10.1093/molbev/msaa121.
Placentation evolved many times independently in vertebrates. Although the core functions of all placentas are similar, we know less about how this similarity extends to the molecular level. Here, we study Poeciliopsis, a unique genus of live-bearing fish that have independently evolved complex placental structures at least three times. The maternal follicle is a key component of these structures. It envelops yolk-rich eggs and is morphologically simple in lecithotrophic species but has elaborate villous structures in matrotrophic species. Through sequencing, the follicle transcriptome of a matrotrophic, Poeciliopsis retropinna, and lecithotrophic, P. turrubarensis, species we found genes known to be critical for placenta function expressed in both species despite their difference in complexity. Additionally, when we compare the transcriptome of different river populations of P. retropinna, known to vary in maternal provisioning, we find differential expression of secretory genes expressed specifically in the top layer of villi cells in the maternal follicle. This provides some of the first evidence that the placental structures of Poeciliopsis function using a secretory mechanism rather than direct contact with maternal circulation. Finally, when we look at the expression of placenta proteins at the maternal-fetal interface of a larger sampling of Poeciliopsis species, we find expression of key maternal and fetal placenta proteins in their cognate tissue types of all species, but follicle expression of prolactin is restricted to only matrotrophic species. Taken together, we suggest that all Poeciliopsis follicles are poised for placenta function but require expression of key genes to form secretory villi.
胎盘在脊椎动物中多次独立进化。虽然所有胎盘的核心功能相似，但我们对这种相似性在分子水平上如何延伸知之甚少。在这里，我们研究了 Poeciliopsis，这是一种独特的卵胎生鱼类属，至少独立进化出了三次复杂的胎盘结构。滤泡是这些结构的关键组成部分。它包裹着富含卵黄的卵子，在卵生鱼类中形态简单，但在胎生鱼类中具有精细的绒毛状结构。通过测序，我们发现了一种胎生的 Poeciliopsis retropinna 和一种卵生的 P. turrubarensis 的滤泡转录组，尽管它们的结构复杂程度不同，但这两个物种都表达了已知对胎盘功能至关重要的基因。此外，当我们比较 P. retropinna 的不同河流种群的转录组时，已知这些种群在母体供应方面存在差异，我们发现了在母体滤泡的绒毛细胞的顶层特异性表达的分泌基因的差异表达。这提供了一些首次证据表明，Poeciliopsis 的胎盘结构使用分泌机制而不是直接与母体循环接触来发挥功能。最后，当我们观察更大的 Poeciliopsis 物种样本的母体-胎儿界面的胎盘蛋白表达时，我们发现所有物种的关键母体和胎儿胎盘蛋白都在其同源组织类型中表达，但只有胎生物种的滤泡表达催乳素。综上所述，我们认为所有的 Poeciliopsis 滤泡都有可能发挥胎盘功能，但需要表达关键基因才能形成分泌性绒毛。
