Ecdysteroid-dependent molting in tardigrades.

IF 8.1 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY
Current Biology Pub Date : 2024-12-16 Epub Date: 2024-11-19 DOI:10.1016/j.cub.2024.10.054
Shumpei Yamakawa, Andreas Hejnol
{"title":"Ecdysteroid-dependent molting in tardigrades.","authors":"Shumpei Yamakawa, Andreas Hejnol","doi":"10.1016/j.cub.2024.10.054","DOIUrl":null,"url":null,"abstract":"<p><p>Although molting is a defining feature of the most species-rich animal taxa-the Ecdysozoa, including arthropods, tardigrades, nematodes, and others<sup>1</sup><sup>,</sup><sup>2</sup>-its evolutionary background remains enigmatic. In pancrustaceans, such as insects and decapods, molting is regulated by the ecdysteroid (Ecd) hormone and its downstream cascade (Figure 1A, see also the text).<sup>3</sup><sup>,</sup><sup>4</sup><sup>,</sup><sup>5</sup> However, whether Ecd-dependent molting predates the emergence of the arthropods and represents an ancestral machinery in ecdysozoans remains unclear. For example, involvement of the Ecd hormone in molting regulation has been suggested only in some parasitic nematodes outside of arthropods,<sup>6</sup><sup>,</sup><sup>7</sup> and insect Ecd synthesis and receptor genes are lacking in some ecysozoan lineages (Figure S1A).<sup>8</sup><sup>,</sup><sup>9</sup><sup>,</sup><sup>10</sup> In this study, we investigated the role of Ecd in the molting process of the tardigrade Hypsibius exemplaris. We show that the endogenous Ecd level periodically increases during the molting cycle of H. exemplaris. The pulse treatment with exogenous Ecd induced molting, whereas an antagonist of the Ecd receptor suppressed the molting. Our spatial and temporal gene expression analysis revealed the putative regulatory organs and Ecd downstream cascades. We demonstrate that tardigrade molting is regulated by the Ecd hormone, supporting the ancestry of Ecd-dependent molting in panarthropods. Furthermore, we were able to identify the putative neural center of molting regulation in tardigrades. This region may be homologous to the neural center in the protocerebrum of pancrustaceans and represent an ancestral state of panarthropods. Together, our results suggest that Ecd-dependent molting evolved in the early-late Ediacaran, 22-76 million years earlier than previously suggested.<sup>11</sup>.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":"5804-5812.e4"},"PeriodicalIF":8.1000,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Current Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.cub.2024.10.054","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/11/19 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Although molting is a defining feature of the most species-rich animal taxa-the Ecdysozoa, including arthropods, tardigrades, nematodes, and others1,2-its evolutionary background remains enigmatic. In pancrustaceans, such as insects and decapods, molting is regulated by the ecdysteroid (Ecd) hormone and its downstream cascade (Figure 1A, see also the text).3,4,5 However, whether Ecd-dependent molting predates the emergence of the arthropods and represents an ancestral machinery in ecdysozoans remains unclear. For example, involvement of the Ecd hormone in molting regulation has been suggested only in some parasitic nematodes outside of arthropods,6,7 and insect Ecd synthesis and receptor genes are lacking in some ecysozoan lineages (Figure S1A).8,9,10 In this study, we investigated the role of Ecd in the molting process of the tardigrade Hypsibius exemplaris. We show that the endogenous Ecd level periodically increases during the molting cycle of H. exemplaris. The pulse treatment with exogenous Ecd induced molting, whereas an antagonist of the Ecd receptor suppressed the molting. Our spatial and temporal gene expression analysis revealed the putative regulatory organs and Ecd downstream cascades. We demonstrate that tardigrade molting is regulated by the Ecd hormone, supporting the ancestry of Ecd-dependent molting in panarthropods. Furthermore, we were able to identify the putative neural center of molting regulation in tardigrades. This region may be homologous to the neural center in the protocerebrum of pancrustaceans and represent an ancestral state of panarthropods. Together, our results suggest that Ecd-dependent molting evolved in the early-late Ediacaran, 22-76 million years earlier than previously suggested.11.

类蜕皮剂依赖于沙蜥的蜕皮。
尽管蜕皮是物种最丰富的动物类群--包括节肢动物、迟缓类动物、线虫等在内的蜕皮动物类群(Ecdysozoa)1,2--的一个决定性特征,但其进化背景仍然令人费解。在昆虫和十足目动物等泛壳类动物中,蜕皮受蜕皮激素(Ecd)及其下游级联的调控(图 1A,另见正文)。例如,仅有节肢动物以外的一些寄生线虫认为 Ecd 激素参与了蜕皮的调控6,7 ,而且一些蜕皮类动物缺乏昆虫 Ecd 合成和受体基因(图 S1A)8,9,10。我们发现,内源性 Ecd 水平在 H. exemplaris 的蜕皮周期中周期性增加。外源 Ecd 的脉冲处理可诱导蜕皮,而 Ecd 受体的拮抗剂则可抑制蜕皮。我们的时空基因表达分析揭示了假定的调控器官和 Ecd 下游级联。我们证明了迟发型蜕皮受 Ecd 激素的调控,支持了泛节肢动物依赖 Ecd 的蜕皮的起源。此外,我们还确定了迟发型动物蜕皮调控的假定神经中枢。该区域可能与盘壳类动物原脑神经中枢同源,代表了泛节肢动物的祖先状态。总之,我们的研究结果表明,依赖于Ecd的蜕皮进化发生在埃迪卡拉纪早-晚期,比之前认为的早了2,200万-7,600万年。
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
Current Biology
Current Biology 生物-生化与分子生物学
CiteScore
11.80
自引率
2.20%
发文量
869
审稿时长
46 days
期刊介绍: Current Biology is a comprehensive journal that showcases original research in various disciplines of biology. It provides a platform for scientists to disseminate their groundbreaking findings and promotes interdisciplinary communication. The journal publishes articles of general interest, encompassing diverse fields of biology. Moreover, it offers accessible editorial pieces that are specifically designed to enlighten non-specialist readers.
×
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