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. 2016 Sep 6;11(9):e0161608.
doi: 10.1371/journal.pone.0161608. eCollection 2016.

Transcriptomic Changes Associated with Pregnancy in a Marsupial, the Gray Short-Tailed Opossum Monodelphis domestica

Affiliations

Transcriptomic Changes Associated with Pregnancy in a Marsupial, the Gray Short-Tailed Opossum Monodelphis domestica

Victoria Leigh Hansen et al. PLoS One. .

Abstract

Live birth has emerged as a reproductive strategy many times across vertebrate evolution; however, mammals account for the majority of viviparous vertebrates. Marsupials are a mammalian lineage that last shared a common ancestor with eutherians (placental mammals) over 148 million years ago. Marsupials are noted for giving birth to highly altricial young after a short gestation, and represent humans' most distant viviparous mammalian relatives. Here we ask what insight can be gained into the evolution of viviparity in mammals specifically and vertebrates in general by analyzing the global uterine transcriptome in a marsupial. Transcriptome analyses were performed using NextGen sequencing of uterine RNA samples from the gray short-tailed opossum, Monodelphis domestica. Samples were collected from late stage pregnant, virgin, and non-pregnant experienced breeders. Three different algorithms were used to determine differential expression, and results were confirmed by quantitative PCR. Over 900 opossum gene transcripts were found to be significantly more abundant in the pregnant uterus than non-pregnant, and over 1400 less so. Most with increased abundance were genes related to metabolism, immune systems processes, and transport. This is the first study to characterize the transcriptomic differences between pregnant, non-pregnant breeders, and virgin marsupial uteruses and helps to establish a set of pregnancy-associated genes in the opossum. These observations allowed for comparative analyses of the differentially transcribed genes with other mammalian and non-mammalian viviparous species, revealing similarities in pregnancy related gene expression over 300 million years of amniote evolution.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Global transcriptomic similarities between samples.
Dendrogram of Jensen-Shannon (JS) distances between transcriptomes of replicates with the pregnant (P), virgin (V), and non-pregnant past breeder (N) transcriptomes.
Fig 2
Fig 2. Overlap of genes called as significant in differential expression programs.
Venn diagrams of the numbers of gene transcripts found to be significantly more abundant (A, C, and E) or less abundant (B, D, and F) when comparing the dataset from the P group to N (A and B), V (C and D) and V2 & V3 only (E and F). Genes were tested for differential expression according to Cuffdiff (pink), DESeq (yellow), and edgeR (blue). Red triangles denote the cases where at least two out of three programs were in agreement.
Fig 3
Fig 3. Gene transcription levels in P vs N according to differential expression programs compared to qPCR data.
Log2-fold changes in the transcription of membrane cofactor protein (CD46), MAC-inhibitory protein (CD59), interleukin 6 (IL-6), lysosomal-associated membrane protein 1 (LAMP1), and lumican (LUM) in the pregnant group compared to the non-pregnant past breeder group. Log2-fold changes were according to Cuffdiff (pink bars), DESeq (yellow bars), edgeR (blue bars), and qPCR using the Vandesompele method (black bars). Red line indicates the threshold of log2-fold change needed for significance according to the Vandesompele method of relative quantification of qPCR data. * Adjusted p < 0.05 for differential expression programs or >2 log2-fold change for qPCR.
Fig 4
Fig 4. Pregnancy-associated gene sets.
Venn diagrams describing the intersection of genes that were considered differentially transcribed in comparisons of the P group to the N, V, and V2 & V3 control groups. The genes that were differentially transcribed in the P group compared to all three control groups (red circles) were considered to be differentially transcribed at a high level of confidence for this study.

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