Cargando…
Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex
Unisexual animals are commonly found in some polyploid species complexes, and most of these species have had a long evolutionary history. However, their method for avoiding genomic decay remains unclear. The polyploid Carassius complex naturally comprises the sexual amphidiploid C. auratus (crucian...
Autores principales: | , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9486886/ https://www.ncbi.nlm.nih.gov/pubmed/36056821 http://dx.doi.org/10.1093/molbev/msac188 |
_version_ | 1784792378514604032 |
---|---|
author | Lu, Meng Li, Zhi Zhu, Zi-Yu Peng, Fang Wang, Yang Li, Xi-Yin Wang, Zhong-Wei Zhang, Xiao-Juan Zhou, Li Gui, Jian-Fang |
author_facet | Lu, Meng Li, Zhi Zhu, Zi-Yu Peng, Fang Wang, Yang Li, Xi-Yin Wang, Zhong-Wei Zhang, Xiao-Juan Zhou, Li Gui, Jian-Fang |
author_sort | Lu, Meng |
collection | PubMed |
description | Unisexual animals are commonly found in some polyploid species complexes, and most of these species have had a long evolutionary history. However, their method for avoiding genomic decay remains unclear. The polyploid Carassius complex naturally comprises the sexual amphidiploid C. auratus (crucian carp or goldfish) (AABB) and the gynogenetic amphitriploid C. gibelio (gibel carp) (AAABBB). Recently, we developed a fertile synthetic amphitetraploid (AAAABBBB) male from C. gibelio by incorporating a C. auratus genome. In this study, we generated novel amphitriploids (AAABBB) by backcrossing the amphitetraploid male with the amphidiploid C. auratus. Whole-genome resequencing revealed the genomic changes, including recombination and independent assortment between homologs of C. gibelio and C. auratus. The fertility, sex determination system, oocyte development, and fertilization behaviors of the novel amphitriploids were investigated. Approximately 80% of the novel amphitriploid females recovered the unisexual gynogenesis ability. Intriguingly, two types of primary oocyte (with and without homolog synapsis) were discovered, and their distinct development fates were observed. Type I oocytes entered apoptosis due to improper synaptonemal complex assembly and incomplete double-strand break repair, whereas subsequent type II oocytes bypassed meiosis through an alternative ameiotic pathway to develop into mature eggs. Moreover, gynogenesis was stabilized in their offspring, and a new array of diverse gynogenetic amphitriploid clones was produced. These revealed genomic changes and detailed cytological data provide comprehensive evidence that changes in ploidy drive unisexual and sexual reproduction transition, thereby resulting in genomic diversity and allowing C. gibelio avoid genomic decay. |
format | Online Article Text |
id | pubmed-9486886 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-94868862022-09-20 Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex Lu, Meng Li, Zhi Zhu, Zi-Yu Peng, Fang Wang, Yang Li, Xi-Yin Wang, Zhong-Wei Zhang, Xiao-Juan Zhou, Li Gui, Jian-Fang Mol Biol Evol Discoveries Unisexual animals are commonly found in some polyploid species complexes, and most of these species have had a long evolutionary history. However, their method for avoiding genomic decay remains unclear. The polyploid Carassius complex naturally comprises the sexual amphidiploid C. auratus (crucian carp or goldfish) (AABB) and the gynogenetic amphitriploid C. gibelio (gibel carp) (AAABBB). Recently, we developed a fertile synthetic amphitetraploid (AAAABBBB) male from C. gibelio by incorporating a C. auratus genome. In this study, we generated novel amphitriploids (AAABBB) by backcrossing the amphitetraploid male with the amphidiploid C. auratus. Whole-genome resequencing revealed the genomic changes, including recombination and independent assortment between homologs of C. gibelio and C. auratus. The fertility, sex determination system, oocyte development, and fertilization behaviors of the novel amphitriploids were investigated. Approximately 80% of the novel amphitriploid females recovered the unisexual gynogenesis ability. Intriguingly, two types of primary oocyte (with and without homolog synapsis) were discovered, and their distinct development fates were observed. Type I oocytes entered apoptosis due to improper synaptonemal complex assembly and incomplete double-strand break repair, whereas subsequent type II oocytes bypassed meiosis through an alternative ameiotic pathway to develop into mature eggs. Moreover, gynogenesis was stabilized in their offspring, and a new array of diverse gynogenetic amphitriploid clones was produced. These revealed genomic changes and detailed cytological data provide comprehensive evidence that changes in ploidy drive unisexual and sexual reproduction transition, thereby resulting in genomic diversity and allowing C. gibelio avoid genomic decay. Oxford University Press 2022-09-03 /pmc/articles/PMC9486886/ /pubmed/36056821 http://dx.doi.org/10.1093/molbev/msac188 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Discoveries Lu, Meng Li, Zhi Zhu, Zi-Yu Peng, Fang Wang, Yang Li, Xi-Yin Wang, Zhong-Wei Zhang, Xiao-Juan Zhou, Li Gui, Jian-Fang Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex |
title | Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex |
title_full | Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex |
title_fullStr | Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex |
title_full_unstemmed | Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex |
title_short | Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex |
title_sort | changes in ploidy drive reproduction transition and genomic diversity in a polyploid fish complex |
topic | Discoveries |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9486886/ https://www.ncbi.nlm.nih.gov/pubmed/36056821 http://dx.doi.org/10.1093/molbev/msac188 |
work_keys_str_mv | AT lumeng changesinploidydrivereproductiontransitionandgenomicdiversityinapolyploidfishcomplex AT lizhi changesinploidydrivereproductiontransitionandgenomicdiversityinapolyploidfishcomplex AT zhuziyu changesinploidydrivereproductiontransitionandgenomicdiversityinapolyploidfishcomplex AT pengfang changesinploidydrivereproductiontransitionandgenomicdiversityinapolyploidfishcomplex AT wangyang changesinploidydrivereproductiontransitionandgenomicdiversityinapolyploidfishcomplex AT lixiyin changesinploidydrivereproductiontransitionandgenomicdiversityinapolyploidfishcomplex AT wangzhongwei changesinploidydrivereproductiontransitionandgenomicdiversityinapolyploidfishcomplex AT zhangxiaojuan changesinploidydrivereproductiontransitionandgenomicdiversityinapolyploidfishcomplex AT zhouli changesinploidydrivereproductiontransitionandgenomicdiversityinapolyploidfishcomplex AT guijianfang changesinploidydrivereproductiontransitionandgenomicdiversityinapolyploidfishcomplex |