CONTRIBUTION OF MATERNAL mRNA PROVISIONING TO EMBRYONIC STRESS RESPONSE IN A REEF-BUILDING CORAL

Abstract

Prior to fertilization, mothers provision their oocytes with mRNA that regulates the early stages of development and may additionally include transcripts for proteins that support embryonic stress response early on. At some point during embryogenesis, however, these maternal transcripts are degraded as zygotic transcription activates and intensifies during a phenomenon known as the maternal-to-zygotic transition (MZT). Some evidence suggests that as the MZT progresses, and the effects of maternal transcripts are waning while the zygotic expression is being established, offspring of marine broadcast spawners become more vulnerable to environmental perturbations. In light of escalating threats to marine broadcast spawners, it is critical to understand their reproduction and development, which are essential processes for species resilience by repopulating and replenishing existing populations. Reef building corals, in particular, are under threat from multiple stressors at the local and global scales. Mass mortality has occurred in recent years due to a series of marine heatwaves. In addition, there is chronic stress occurring in the form of ocean acidification, or the decline in pH in surface waters due to the uptake of atmospheric carbon dioxide of anthropogenic origin. Here, we characterize the function of maternal mRNAs, the timeline of the MZT, and sensitivity of gene expression to ocean acidification (OA) in the reef- building coral, Montipora capitata to investigate role of the MZT in embryonic stress response in reef-building corals. In Manuscript 1, we examine gene expression over nine developmental stages in Montipora capitata from eggs and embryos at 1, 4, 9, 14, 22, and 36 hours-post-fertilization (hpf), as well as swimming larvae (9d), and adult colonies. Weighted 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 enzymes (TET1) peak and remain