Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in the reef-building coral Montipora capitata
Chille E 1, Strand E 1, Neder M 2, Schmidt V 3, Sherman M 1, Mass T 2, Putnam HM 1
1 Department of Biology, University of Rhode Island, Rhode Island, USA
2 Department of Marine Biology, The Leon H. Charney School of Marine Sciences, University of Haifa, Haifa, Israel
3 Yale School of Medicine, Yale University, Connecticut, USA
This repository provides data and scripts to analyze Monitpora capitata gene expression dynamics across nine life stages from pre-fertilization to adult, focusing on shifts in the gene expression network within the first 24 hours post-spawning. This analysis provides data characterizing the coral maternal mRNA complement, as well as transcriptome and epigenetic reprogramming dynamics during the Maternal to Zygotic transition (MZT).
Prior to fertilization, mothers provision their oocytes with mRNA that regulates the early stages of development. At some point during embryogenesis, these maternal transcripts are degraded as zygotic transcription activates and intensifies, a phenomenon known as the maternal-to-zygotic transition (MZT). Here, we examine changes in gene expression over nine developmental stages ranging from unfertilized egg to adults in the Pacific rice coral, Montipora capitata. In order to elucidate maternal provisioning and the maternal-to-zygotic transition, mRNA was sequenced from eggs and embryos at 1, 4, 9, 14, 22, and 36 hours post-fertilization (hpf), as well as swimming larvae (9 days), and adults (>years). Weighted Gene Coexpression Network Analysis (WGCNA) identified nine clusters of co-expression modules that revealed four main peaks in expression, thereby identifying the maternal complement, the first wave of the MZT, the second wave of the MZT, and adult expression patterns. These patterns identify that in M. capitata, the maternal transition is initiated during cleavage and continues through late gastrulation in two waves. Functional gene ontology enrichment analysis and semantic similarity clustering revealed the maternal mRNAs were dominated by cell division, methylation, biosynthesis, metabolism, and protein/RNA processing and transport functions. Initiation of zygotic genome activation (ZGA) starts with aThe first wave, from 4hpf through 14hpf, which is characterized by degradation of maternal mRNA.The first wave of the MZT continued to be dominated by terms related to biosynthesis, methylation, and cell division, in addition to transcription. In contrast, functional enrichment in the second MTZ wave, from 22hpf to 9 days, is enriched for the expression of genes related primarily to ion/peptide transport and cell signaling. Finally, the adult expression pattern was enriched for genes with functions related to signaling, metabolism, and ion/peptide transport. Our four phases of expression are further supported by the expression patterns of key enzymes involved in bauplan specification (Brachyury and WNT8) which peak during early and late gastrulation. Further, we elucidated the patterns of DNA methylation writing (DNA methyltransferase 3a) and removing enzymes (Ten Eleven Translocation) that peak at cleavage (4hpf) and prawn chip (9hpf) stages, respectively. Our results provide high-resolution insight into maternal provisioning and the maternal-to-zygotic transition. We hypothesize would expect specific sensitivity of gene expression to stressors begins around early gastrulation (~14 hpf) along with the ZGA initiation. Characterization of the coral maternal mRNA complement in the eggs and MZT provides essential information regarding setting the stage for, and the sensitivity of, developmental success and potential parental carryover effects under increasing environmental stressors.
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