The evolution of gene expression in mammalian organ development remains largely uncharacterized. Here we report the transcriptomes of seven organs (cerebrum, cerebellum, heart, kidney, liver, ovary and testis) across developmental time points from early organogenesis to adulthood for human, macaque, mouse, rat, rabbit, opossum and chicken. Comparisons of gene expression patterns identified developmental stage correspondences across species, and differences in the timing of key events during the development of the gonads. We found that the breadth of gene expression and the extent of purifying selection gradually decrease during development, whereas the amount of positive selection and expression of new genes increase. We identified differences in the temporal trajectories of expression of individual genes across species, with brain tissues showing the smallest percentage of trajectory changes, and the liver and testis showing the largest. Our work provides a resource of developmental transcriptomes of seven organs across seven species, and comparative analyses that characterize the development and evolution of mammalian organs.
The mammalian placenta is remarkably distinct between species, suggesting a history of rapid evolutionary diversification1. To gain insight into the molecular drivers of placental evolution, we compared biochemically predicted enhancers between mouse and rat trophoblast stem cells (TSCs) and find that species-specific enhancers are highly enriched for endogenous retroviruses (ERVs) on a genome-wide level. One of these ERV families, RLTR13D5, contributes hundreds of mouse-specific H3K4me1/H3K27ac-defined enhancers that functionally bind Cdx2, Eomes, and Elf5 - core factors that define the TSC regulatory network. Furthermore, we demonstrate that RLTR13D5 is capable of driving gene expression in rat placental cells. Comparison with other tissues revealed that species-specific ERV enhancer activity is generally restricted to hypomethylated tissues, suggesting that tissues permissive to ERV activity gain access to an otherwise silenced source of regulatory variation. Overall, our results implicate ERV enhancer cooption as a mechanism underlying the striking evolutionary diversification of placental development.
Leaders gathered at the US National Institutes of Health in November 2014 to discuss recent advances and emerging research areas in aspects of maternal-fetal immunity that may affect fetal development and pregnancy success.
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