Insights from the transcriptome of the elephant and the origin of eutherian placentation. Loxodonta africana

The placenta is essential for fetal growth and development in all mammal species that bear live offspring. In most eutherians the placenta is invasive and this distinguishes the organ from placentas in other animals. Understanding the evolutionary history of the placenta is aided by cross-species studies of expressed genes. The African elephant belongs to the clade of placental mammals most distantly related to humans; therefore, we chose to sequence its placental transcriptome as a means of shedding light on the diversity of mammalian placentation. We sequenced 524,115 reads derived from transcripts of the elephant placenta and assembled the reads into 55,409 contigs. The mean length of these assembled contigs is 284bp, and the average fold sequence coverage per contig is 7.0X. From these data we provide evidence that ~10% (5874/55910) of elephant contigs are orthologous to 5126 genes that are also expressed in mouse and human placenta. This finding suggests that there is a common placenta transcriptional pattern shared among eutherian mammals. We also describe lineage specific transcripts in human, mouse, cow and elephant. The 10 abundant and long novel transcripts in the elephant placenta were experimentally confirmed by traditional sequencing of RT-PCR products, and this suggests our analysis methods are effective for discovering species-specific transcripts. Using comparative genomics, we found that the majority of genes commonly expressed in eutherian mammal placentas existed before the origin of the eutherian placenta (Fisher exact test, P=1×10-16). We further propose that while lineage-specific transcripts may have contributed to the anatomical and developmental variation seen in the placentas of diverse mammalian species it is commonly expressed genes in the eutherian placenta that represent the core genetic elements responsible for placenta ontogeny.