Abstract
BackgroundMaternal mRNA provisioning of oocytes regulates early embryogenesis. Maternal transcripts are degraded as zygotic genome activation (ZGA) intensifies, a phenomenon known as the maternal-to-zygotic transition (MZT). Here, we examine gene expression over nine developmental stages in the Pacific rice coral, Montipora capitata, from eggs and embryos at 1, 4, 9, 14, 22, and 36 h-post-fertilization (hpf), as well as swimming larvae (9d), and adult colonies.ResultsWeighted Gene Coexpression Network Analysis revealed four expression peaks, identifying the maternal complement, two waves of the MZT, and adult expression. Gene ontology enrichment revealed maternal mRNAs are dominated by cell division, methylation, biosynthesis, metabolism, and protein/RNA processing and transport functions. The first MZT wave occurs from ~4-14 hpf and is enriched in terms related to biosynthesis, methylation, cell division, and transcription. In contrast, functional enrichment in the second MZT wave, or ZGA, from 22 hpf-9dpf, includes ion/peptide transport and cell signaling. Finally, adult expression is enriched for functions related to signaling, metabolism, and ion/peptide transport. Our proposed MZT timing is further supported by expression of enzymes involved in zygotic transcriptional repression (Kaiso) and activation (Sox2), which peak at 14 hpf and 22 hpf, respectively. Further, DNA methylation writing (DNMT3a) and removing (TET1) enzymes peak and remain stable past ~4 hpf, suggesting that methylome programming occurs before 4 hpf.ConclusionsOur high-resolution insight into the coral maternal mRNA and MZT provides essential baseline information to understand parental carryover effects and the sensitivity of developmental success under increasing environmental stress.
Highlights
Maternal mRNA provisioning of oocytes regulates early embryogenesis
Weighted Gene Co-expression Network Analysis (WGCNA) facilitated the identification of the maternal mRNA complement, two waves of zygotic genome activation (ZGA), and adult expression
Maternal provisioning The active maternal mRNA complement, here defined as the modules significantly positively correlated with either the unfertilized and fertilized egg samples, was enriched in biological processes primarily related to housekeeping functions
Summary
Maternal mRNA provisioning of oocytes regulates early embryogenesis. Maternal transcripts are degraded as zygotic genome activation (ZGA) intensifies, a phenomenon known as the maternal-to-zygotic transition (MZT). Over the course of hours to days, embryos develop into planula larvae [10] and may spend several hours to weeks in the water column, or searching the benthos for an appropriate location to settle and metamorphose into coral spat [11]. This prolonged pelagic period constitutes an ontogenetic bottleneck for corals and other broadcast-spawning marine organisms, during which they are sensitive to climate-related stressors [6, 7]. The cumulative effects of these unprecedented stressors on early development may compromise recruitment, the process in which offspring repopulate and replenish declining populations, further contributing to the destabilization of coral reef ecosystems [2]
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