Vladimir A Timoshevskiy, Nataliya Timoshevskaya, Kaan I Eşkut, Kasturi Rajandran, Jeramiah J Smith
{"title":"海七鳃鳗种系特异性染色体的双亲遗传及其在卵母细胞中的作用。","authors":"Vladimir A Timoshevskiy, Nataliya Timoshevskaya, Kaan I Eşkut, Kasturi Rajandran, Jeramiah J Smith","doi":"10.1073/pnas.2421883122","DOIUrl":null,"url":null,"abstract":"<p><p>Many eukaryotic species undergo programmed elimination of specific chromosomes during embryogenesis, typically retaining these chromosomes only in their germ cells. In some species, programmatic elimination of GRCs, or sex chromosomes, also occurs in a sex-specific manner, with specific chromosomes being transmitted or eliminated by only one sex. As such, these chromosomes provide a unique perspective on the evolution of gene functions that are advantageous to the germline and genetic tradeoffs between somatic vs germline or oocyte vs sperm biology. While GRCs have been extensively characterized in male sea lampreys (<i>Petromyzon marinus</i>), the status of GRCs in females has not yet been resolved, though it has been hypothesized that male-specific expression/transmission of these chromosomes might provide a solution to resolving the long-standing mystery of lamprey sex determining mechanisms. To gain insight into the roles of GRCs in female lampreys, we performed several karyological, transcriptomic, and genomic analyses, which demonstrate that GRCs are present in the female lamprey germline, transmitted by oocytes and somatically eliminated in both sexes. These analyses also show that GRCs play important roles in the maintenance and development of female germline but provide no evidence for sex-specific variation in the elimination and transmission of lamprey GRCs. These findings underscore the diversity of germline functions that are carried out by GRCs in both male and female lampreys and highlight the fact that sex-specific transmission/retention of GRCs likely follows no universal rules across the diverse lineages that have independently evolved to undergo developmentally programmed DNA elimination.</p>","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"122 24","pages":"e2421883122"},"PeriodicalIF":9.1000,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12184396/pdf/","citationCount":"0","resultStr":"{\"title\":\"Biparental inheritance of germline-specific chromosomes in the sea lamprey and their roles in oocytes.\",\"authors\":\"Vladimir A Timoshevskiy, Nataliya Timoshevskaya, Kaan I Eşkut, Kasturi Rajandran, Jeramiah J Smith\",\"doi\":\"10.1073/pnas.2421883122\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Many eukaryotic species undergo programmed elimination of specific chromosomes during embryogenesis, typically retaining these chromosomes only in their germ cells. In some species, programmatic elimination of GRCs, or sex chromosomes, also occurs in a sex-specific manner, with specific chromosomes being transmitted or eliminated by only one sex. As such, these chromosomes provide a unique perspective on the evolution of gene functions that are advantageous to the germline and genetic tradeoffs between somatic vs germline or oocyte vs sperm biology. While GRCs have been extensively characterized in male sea lampreys (<i>Petromyzon marinus</i>), the status of GRCs in females has not yet been resolved, though it has been hypothesized that male-specific expression/transmission of these chromosomes might provide a solution to resolving the long-standing mystery of lamprey sex determining mechanisms. To gain insight into the roles of GRCs in female lampreys, we performed several karyological, transcriptomic, and genomic analyses, which demonstrate that GRCs are present in the female lamprey germline, transmitted by oocytes and somatically eliminated in both sexes. These analyses also show that GRCs play important roles in the maintenance and development of female germline but provide no evidence for sex-specific variation in the elimination and transmission of lamprey GRCs. These findings underscore the diversity of germline functions that are carried out by GRCs in both male and female lampreys and highlight the fact that sex-specific transmission/retention of GRCs likely follows no universal rules across the diverse lineages that have independently evolved to undergo developmentally programmed DNA elimination.</p>\",\"PeriodicalId\":20548,\"journal\":{\"name\":\"Proceedings of the National Academy of Sciences of the United States of America\",\"volume\":\"122 24\",\"pages\":\"e2421883122\"},\"PeriodicalIF\":9.1000,\"publicationDate\":\"2025-06-17\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12184396/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Proceedings of the National Academy of Sciences of the United States of America\",\"FirstCategoryId\":\"103\",\"ListUrlMain\":\"https://doi.org/10.1073/pnas.2421883122\",\"RegionNum\":1,\"RegionCategory\":\"综合性期刊\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2025/6/12 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"MULTIDISCIPLINARY SCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Proceedings of the National Academy of Sciences of the United States of America","FirstCategoryId":"103","ListUrlMain":"https://doi.org/10.1073/pnas.2421883122","RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/6/12 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"MULTIDISCIPLINARY SCIENCES","Score":null,"Total":0}
Biparental inheritance of germline-specific chromosomes in the sea lamprey and their roles in oocytes.
Many eukaryotic species undergo programmed elimination of specific chromosomes during embryogenesis, typically retaining these chromosomes only in their germ cells. In some species, programmatic elimination of GRCs, or sex chromosomes, also occurs in a sex-specific manner, with specific chromosomes being transmitted or eliminated by only one sex. As such, these chromosomes provide a unique perspective on the evolution of gene functions that are advantageous to the germline and genetic tradeoffs between somatic vs germline or oocyte vs sperm biology. While GRCs have been extensively characterized in male sea lampreys (Petromyzon marinus), the status of GRCs in females has not yet been resolved, though it has been hypothesized that male-specific expression/transmission of these chromosomes might provide a solution to resolving the long-standing mystery of lamprey sex determining mechanisms. To gain insight into the roles of GRCs in female lampreys, we performed several karyological, transcriptomic, and genomic analyses, which demonstrate that GRCs are present in the female lamprey germline, transmitted by oocytes and somatically eliminated in both sexes. These analyses also show that GRCs play important roles in the maintenance and development of female germline but provide no evidence for sex-specific variation in the elimination and transmission of lamprey GRCs. These findings underscore the diversity of germline functions that are carried out by GRCs in both male and female lampreys and highlight the fact that sex-specific transmission/retention of GRCs likely follows no universal rules across the diverse lineages that have independently evolved to undergo developmentally programmed DNA elimination.
期刊介绍:
The Proceedings of the National Academy of Sciences (PNAS), a peer-reviewed journal of the National Academy of Sciences (NAS), serves as an authoritative source for high-impact, original research across the biological, physical, and social sciences. With a global scope, the journal welcomes submissions from researchers worldwide, making it an inclusive platform for advancing scientific knowledge.