Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral

Abstract Background 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). Here, we examine gene expression over nine developmental stages i...

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Autores principales:	Erin Chille, Emma Strand, Mayaan Neder, Valeria Schmidt, Madeleine Sherman, Tali Mass, Hollie Putnam
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Time course WGCNA Epigenetics Resilience Oocyte Embryo Biotechnology TP248.13-248.65 Genetics QH426-470
Acceso en línea:	https://doaj.org/article/abb716c4dfa643cca776bed4dc3bd248
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spelling	oai:doaj.org-article:abb716c4dfa643cca776bed4dc3bd2482021-11-14T12:26:58ZDevelopmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral10.1186/s12864-021-08114-y1471-2164https://doaj.org/article/abb716c4dfa643cca776bed4dc3bd2482021-11-01T00:00:00Zhttps://doi.org/10.1186/s12864-021-08114-yhttps://doaj.org/toc/1471-2164Abstract Background 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). 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. Results 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 (TET1) enzymes peak and remain stable past ~4 hpf, suggesting that methylome programming occurs before 4 hpf. Conclusions Our 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.Erin ChilleEmma StrandMayaan NederValeria SchmidtMadeleine ShermanTali MassHollie PutnamBMCarticleTime courseWGCNAEpigeneticsResilienceOocyteEmbryoBiotechnologyTP248.13-248.65GeneticsQH426-470ENBMC Genomics, Vol 22, Iss 1, Pp 1-17 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Time course WGCNA Epigenetics Resilience Oocyte Embryo Biotechnology TP248.13-248.65 Genetics QH426-470
spellingShingle	Time course WGCNA Epigenetics Resilience Oocyte Embryo Biotechnology TP248.13-248.65 Genetics QH426-470 Erin Chille Emma Strand Mayaan Neder Valeria Schmidt Madeleine Sherman Tali Mass Hollie Putnam Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral
description	Abstract Background 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). 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. Results 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 (TET1) enzymes peak and remain stable past ~4 hpf, suggesting that methylome programming occurs before 4 hpf. Conclusions Our 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.
format	article
author	Erin Chille Emma Strand Mayaan Neder Valeria Schmidt Madeleine Sherman Tali Mass Hollie Putnam
author_facet	Erin Chille Emma Strand Mayaan Neder Valeria Schmidt Madeleine Sherman Tali Mass Hollie Putnam
author_sort	Erin Chille
title	Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral
title_short	Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral
title_full	Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral
title_fullStr	Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral
title_full_unstemmed	Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral
title_sort	developmental series of gene expression clarifies maternal mrna provisioning and maternal-to-zygotic transition in a reef-building coral
publisher	BMC
publishDate	2021
url	https://doaj.org/article/abb716c4dfa643cca776bed4dc3bd248
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Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral

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