Transcriptional regulation analysis reveals the complexity of metamorphosis in the Pacific oyster (Crassostrea gigas).

IF 5.8 2区 生物学 Q1 MARINE & FRESHWATER BIOLOGY
Marine Life Science & Technology Pub Date : 2023-11-25 eCollection Date: 2023-11-01 DOI:10.1007/s42995-023-00204-y
Fei Xu, Shaoxi Deng, Daria Gavriouchkina, Guofan Zhang
{"title":"Transcriptional regulation analysis reveals the complexity of metamorphosis in the Pacific oyster (<i>Crassostrea gigas</i>).","authors":"Fei Xu, Shaoxi Deng, Daria Gavriouchkina, Guofan Zhang","doi":"10.1007/s42995-023-00204-y","DOIUrl":null,"url":null,"abstract":"<p><p>Many marine invertebrate phyla are characterized by indirect development. These animals transit from planktonic larvae to benthic spats via settlement and metamorphosis, which contributes to their adaption to the marine environment. Studying the biological process of metamorphosis is, thus, key to understanding the origin and evolution of indirect development. Although numerous studies have been conducted on the relationship between metamorphosis and the marine environment, microorganisms, and neurohormones, little is known about gene regulation network (GRN) dynamics during metamorphosis. Metamorphosis-competent pediveligers of the Pacific oyster <i>Crassostrea gigas</i> were assayed in this study. By assaying gene expression patterns and open chromatin region changes of different samples of larvae and spats, the dynamics of molecular regulation during metamorphosis were examined. The results indicated significantly different gene regulation networks before, during and post-metamorphosis. Genes encoding membrane-integrated receptors and those related to the remodeling of the nervous system were upregulated before the initiation of metamorphosis. Massive biogenesis, e.g., of various enzymes and structural proteins, occurred during metamorphosis as inferred from the comprehensive upregulation of the protein synthesis system post epinephrine stimulation. Hierarchical downstream gene networks were then stimulated. Some transcription factors, including homeobox, basic helix-loop-helix and nuclear receptors, showed different temporal response patterns, suggesting a complex GRN during the transition stage. Nuclear receptors, as well as their retinoid X receptor partner, may participate in the GRN controlling oyster metamorphosis, indicating an ancient role of the nuclear receptor regulation system in animal metamorphosis.</p><p><strong>Supplementary information: </strong>The online version contains supplementary material available at 10.1007/s42995-023-00204-y.</p>","PeriodicalId":53218,"journal":{"name":"Marine Life Science & Technology","volume":null,"pages":null},"PeriodicalIF":5.8000,"publicationDate":"2023-11-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689616/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Marine Life Science & Technology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1007/s42995-023-00204-y","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2023/11/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"MARINE & FRESHWATER BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Many marine invertebrate phyla are characterized by indirect development. These animals transit from planktonic larvae to benthic spats via settlement and metamorphosis, which contributes to their adaption to the marine environment. Studying the biological process of metamorphosis is, thus, key to understanding the origin and evolution of indirect development. Although numerous studies have been conducted on the relationship between metamorphosis and the marine environment, microorganisms, and neurohormones, little is known about gene regulation network (GRN) dynamics during metamorphosis. Metamorphosis-competent pediveligers of the Pacific oyster Crassostrea gigas were assayed in this study. By assaying gene expression patterns and open chromatin region changes of different samples of larvae and spats, the dynamics of molecular regulation during metamorphosis were examined. The results indicated significantly different gene regulation networks before, during and post-metamorphosis. Genes encoding membrane-integrated receptors and those related to the remodeling of the nervous system were upregulated before the initiation of metamorphosis. Massive biogenesis, e.g., of various enzymes and structural proteins, occurred during metamorphosis as inferred from the comprehensive upregulation of the protein synthesis system post epinephrine stimulation. Hierarchical downstream gene networks were then stimulated. Some transcription factors, including homeobox, basic helix-loop-helix and nuclear receptors, showed different temporal response patterns, suggesting a complex GRN during the transition stage. Nuclear receptors, as well as their retinoid X receptor partner, may participate in the GRN controlling oyster metamorphosis, indicating an ancient role of the nuclear receptor regulation system in animal metamorphosis.

Supplementary information: The online version contains supplementary material available at 10.1007/s42995-023-00204-y.

转录调控分析揭示了太平洋牡蛎(长牡蛎)变态的复杂性。
许多海洋无脊椎动物门具有间接发育的特点。这些动物通过定居和变态从浮游幼虫转变为底栖动物,这有助于它们适应海洋环境。因此,研究变态的生物学过程是理解间接发育起源和演化的关键。虽然关于变态与海洋环境、微生物和神经激素之间的关系已经进行了大量的研究,但对变态过程中基因调控网络(GRN)的动态知之甚少。本研究对具有蜕变能力的太平洋牡蛎长牡蛎幼体进行了研究。通过分析不同样品的基因表达模式和开放染色质区域的变化,探讨了幼虫和幼体在变态过程中的分子调控动态。结果表明,在变态前、变态中、变态后基因调控网络存在显著差异。编码膜整合受体的基因和与神经系统重塑相关的基因在变态开始前被上调。从肾上腺素刺激后蛋白质合成系统的全面上调推断,在变态过程中发生了大量的生物发生,例如各种酶和结构蛋白。层级下游基因网络随后受到刺激。同源盒型、碱性螺旋-环-螺旋和核受体等转录因子表现出不同的时间响应模式,表明在过渡阶段存在复杂的GRN。核受体及其类视黄醇X受体伴侣可能参与了GRN对牡蛎变态的控制,这表明核受体调控系统在动物变态中具有古老的作用。补充信息:在线版本包含补充资料,下载地址:10.1007/s42995-023-00204-y。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Marine Life Science & Technology
Marine Life Science & Technology MARINE & FRESHWATER BIOLOGY-
CiteScore
9.60
自引率
10.50%
发文量
58
期刊介绍: Marine Life Science & Technology (MLST), established in 2019, is dedicated to publishing original research papers that unveil new discoveries and theories spanning a wide spectrum of life sciences and technologies. This includes fundamental biology, fisheries science and technology, medicinal bioresources, food science, biotechnology, ecology, and environmental biology, with a particular focus on marine habitats. The journal is committed to nurturing synergistic interactions among these diverse disciplines, striving to advance multidisciplinary approaches within the scientific field. It caters to a readership comprising biological scientists, aquaculture researchers, marine technologists, biological oceanographers, and ecologists.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信