Meiosis I causes a high spontaneous mutation rate in a multicellular red alga (Pyropia yezoensis) with a complex life cycle

IF 4.6 2区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Algal Research-Biomass Biofuels and Bioproducts Pub Date : 2024-09-10 DOI:10.1016/j.algal.2024.103694
Xinzi Yu , Xianghai Tang , Kuipeng Xu , Lu Wang , Yunxiang Mao
{"title":"Meiosis I causes a high spontaneous mutation rate in a multicellular red alga (Pyropia yezoensis) with a complex life cycle","authors":"Xinzi Yu ,&nbsp;Xianghai Tang ,&nbsp;Kuipeng Xu ,&nbsp;Lu Wang ,&nbsp;Yunxiang Mao","doi":"10.1016/j.algal.2024.103694","DOIUrl":null,"url":null,"abstract":"<div><p>Mutations are the origin of genetic diversity and are fundamental parameters needed to understand the molecular evolution of species. Estimations of mutation rates have been conducted for many diverse taxa, although rates in several major eukaryotic lineages remain unexplored. Here, the first estimation is reported of the spontaneous mutation rate for the multicellular eukaryote red alga, <em>Pyropia yezoensis</em>, which exhibits a complex life cycle. An estimated mutation rate of 2.97 × 10<sup>−8</sup> (95 % CI: 2.16 × 10<sup>−8</sup>–3.99 × 10<sup>−8</sup>) per site per generation was generated for the primary life cycle, the sexual cycle, which is the highest sexual mutation rate among published sexual plants. Combined with tetrad analysis, meiosis I was identified as the primary period responsible for the high mutation rate during the complex life cycle of <em>P. yezoensis</em>. This result provides direct evidence for the “meiosis is mutagenic” hypothesis for multicellular organisms. The accurate estimate of the mutation rate of <em>P. yezoensis</em> also informs several immediate applications. Based on the above estimate, the effective population size (N<sub>e</sub>) of <em>P. yezoensis</em> was estimated at about 19,000, with extensive haploid phases and asexual reproduction through monospores possibly leading to linked selection that may reduce the genome-wide genetic diversity of <em>P. yezoensis</em> and consequently influence N<sub>e</sub> estimation. Lastly, <em>P. yezoensis</em> was estimated to have diverged from <em>P. haitanensis</em> about 4.2 Ma, representing a more recent date than estimates from fossil-calibrated phylogenies. These findings provide valuable new information for understanding the evolution of red algae, in addition to the underlying mechanism of mutations.</p></div>","PeriodicalId":7855,"journal":{"name":"Algal Research-Biomass Biofuels and Bioproducts","volume":"83 ","pages":"Article 103694"},"PeriodicalIF":4.6000,"publicationDate":"2024-09-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S2211926424003060/pdfft?md5=efe1a23f2155dd32dbb825d0dc17c17b&pid=1-s2.0-S2211926424003060-main.pdf","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Algal Research-Biomass Biofuels and Bioproducts","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2211926424003060","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Mutations are the origin of genetic diversity and are fundamental parameters needed to understand the molecular evolution of species. Estimations of mutation rates have been conducted for many diverse taxa, although rates in several major eukaryotic lineages remain unexplored. Here, the first estimation is reported of the spontaneous mutation rate for the multicellular eukaryote red alga, Pyropia yezoensis, which exhibits a complex life cycle. An estimated mutation rate of 2.97 × 10−8 (95 % CI: 2.16 × 10−8–3.99 × 10−8) per site per generation was generated for the primary life cycle, the sexual cycle, which is the highest sexual mutation rate among published sexual plants. Combined with tetrad analysis, meiosis I was identified as the primary period responsible for the high mutation rate during the complex life cycle of P. yezoensis. This result provides direct evidence for the “meiosis is mutagenic” hypothesis for multicellular organisms. The accurate estimate of the mutation rate of P. yezoensis also informs several immediate applications. Based on the above estimate, the effective population size (Ne) of P. yezoensis was estimated at about 19,000, with extensive haploid phases and asexual reproduction through monospores possibly leading to linked selection that may reduce the genome-wide genetic diversity of P. yezoensis and consequently influence Ne estimation. Lastly, P. yezoensis was estimated to have diverged from P. haitanensis about 4.2 Ma, representing a more recent date than estimates from fossil-calibrated phylogenies. These findings provide valuable new information for understanding the evolution of red algae, in addition to the underlying mechanism of mutations.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
减数分裂 I 在具有复杂生命周期的多细胞红藻(Pyropia yezoensis)中导致高自发突变率
突变是遗传多样性的起源,也是了解物种分子进化所需的基本参数。对许多不同类群的突变率进行了估算,但对几个主要真核生物系的突变率仍未进行研究。本文首次估算了多细胞真核红藻 Pyropia yezoensis 的自发突变率,该藻具有复杂的生命周期。在主要生命周期(有性生殖周期)中,估计每一代每个位点的突变率为 2.97 × 10-8(95 % CI:2.16 × 10-8-3.99 × 10-8),这是已发表的有性植物中最高的有性突变率。结合四分体分析,可以确定减数分裂 I 是造成酵母属(P. yezoensis)复杂生命周期高突变率的主要时期。这一结果为多细胞生物的 "减数分裂具有突变性 "假说提供了直接证据。对叶索动物突变率的准确估计也为一些直接应用提供了信息。根据上述估计,酵母藻的有效种群数量(Ne)约为 19,000 个,单倍体阶段和单孢子无性繁殖可能会导致关联选择,从而降低酵母藻的全基因组遗传多样性,进而影响 Ne 的估计。最后,据估计,P. yezoensis 与 P. haitanensis 的分化时间约为 4.2 Ma,比化石校准系统发育所估计的时间更近。这些发现为了解红藻的进化以及变异的内在机制提供了宝贵的新信息。
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 去求助
来源期刊
Algal Research-Biomass Biofuels and Bioproducts
Algal Research-Biomass Biofuels and Bioproducts BIOTECHNOLOGY & APPLIED MICROBIOLOGY-
CiteScore
9.40
自引率
7.80%
发文量
332
期刊介绍: Algal Research is an international phycology journal covering all areas of emerging technologies in algae biology, biomass production, cultivation, harvesting, extraction, bioproducts, biorefinery, engineering, and econometrics. Algae is defined to include cyanobacteria, microalgae, and protists and symbionts of interest in biotechnology. The journal publishes original research and reviews for the following scope: algal biology, including but not exclusive to: phylogeny, biodiversity, molecular traits, metabolic regulation, and genetic engineering, algal cultivation, e.g. phototrophic systems, heterotrophic systems, and mixotrophic systems, algal harvesting and extraction systems, biotechnology to convert algal biomass and components into biofuels and bioproducts, e.g., nutraceuticals, pharmaceuticals, animal feed, plastics, etc. algal products and their economic assessment
期刊最新文献
Deep sequencing analysis of chloroplast transcription and splicing in Euglena gracilis Genetic transformation of the freshwater diatom Cyclotella meneghiniana via bacterial conjugation Comparison of CRISPR/Cas9 and Cas12a for gene editing in Chlamydomonas reinhardtii Effect of temperature on the oxygen production capacity and growth of scenedesmus almeriensis A multi-dimensional comparative study on the performance of algae removal using various flotation
×
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
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 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 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1