Genome-Wide Analysis of Transposable Elements and Satellite DNAs in Spinacia Species to Shed Light on Their Roles in Sex Chromosome Evolution

Sex chromosome evolution has mostly been studied in species with heteromorphic sex chromosomes. The Spinacia genus serves as an ideal model for investigating evolutionary mechanisms underlying the transition from homomorphic to heteromorphic sex chromosomes. Among evolutionary factors, repetitive se...

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Main Authors: Ning Li, Xiaoyue Li, Jian Zhou, Li’ang Yu, Shufen Li, Yulan Zhang, Ruiyun Qin, Wujun Gao, Chuanliang Deng
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2020.575462/full
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spelling doaj-3a2746d1820142748e18add944a1cf1d2021-01-14T04:34:08ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-01-011110.3389/fpls.2020.575462575462Genome-Wide Analysis of Transposable Elements and Satellite DNAs in Spinacia Species to Shed Light on Their Roles in Sex Chromosome EvolutionNing Li0Xiaoyue Li1Jian Zhou2Li’ang Yu3Shufen Li4Yulan Zhang5Ruiyun Qin6Wujun Gao7Chuanliang Deng8College of Life Sciences, Henan Normal University, Xinxiang, ChinaCollege of Life Sciences, Henan Normal University, Xinxiang, ChinaCollege of Life Sciences, Henan Normal University, Xinxiang, ChinaDepartment of Plant Biology, University of Illinois at Urbana-Champaign, Champaign, IL, United StatesCollege of Life Sciences, Henan Normal University, Xinxiang, ChinaCollege of Life Sciences, Henan Normal University, Xinxiang, ChinaCollege of Life Sciences, Henan Normal University, Xinxiang, ChinaCollege of Life Sciences, Henan Normal University, Xinxiang, ChinaCollege of Life Sciences, Henan Normal University, Xinxiang, ChinaSex chromosome evolution has mostly been studied in species with heteromorphic sex chromosomes. The Spinacia genus serves as an ideal model for investigating evolutionary mechanisms underlying the transition from homomorphic to heteromorphic sex chromosomes. Among evolutionary factors, repetitive sequences play multiple roles in sex chromosome evolution while their forces have not been fully explored in Spinacia species. Here, we identified major repetitive sequence classes in male and female genomes of Spinacia species and their ancestral relative sugar beet to elucidate the evolutionary processes of sex chromosome evolution using next-generation sequencing (NGS) data. Comparative analysis revealed that the repeat elements of Spinacia species are considerably higher than of sugar beet, especially the Ty3/Gypsy and Ty1/Copia retrotransposons. The long terminal repeat retroelements (LTR) Angela, Athila, and Ogre may be accounted for the higher proportion of repeats in the spinach genome. Comparison of the repeats proportion between female and male genomes of three Spinacia species indicated the different representation in Spinacia tetrandra samples but not in the S. oleracea or S. turkestanica samples. From these results, we speculated that emergence of repetitive DNA sequences may correlate the formation of sex chromosome and the transition from homomorphic sex chromosomes to heteromorphic sex chromosomes as heteromorphic sex chromosomes exclusively existed in Spinacia tetrandra. Three novel sugar beet-specific satellites were identified and confirmed by fluorescence in situ hybridization (FISH); six out of eight new spinach-specific satellites were mapped to the short arm of sex chromosomes. A total of 141 copies of SolSat01-171-s were found in the sex determination region (SDR). Thus, the accumulation of satellite DNA on the short arm of chromosome 1 may be involved in the sex chromosome evolution in Spinacia species. Our study provides a fundamental resource for understanding repeat sequences in Spinacia species and their roles in sex chromosome evolution.https://www.frontiersin.org/articles/10.3389/fpls.2020.575462/fullrepetitive DNA sequencesrDNAhomomorphic sex chromosomeheteromorphic sex chromosomelong terminal repeat retroelementsnext generation sequencing
collection DOAJ
language English
format Article
sources DOAJ
author Ning Li
Xiaoyue Li
Jian Zhou
Li’ang Yu
Shufen Li
Yulan Zhang
Ruiyun Qin
Wujun Gao
Chuanliang Deng
spellingShingle Ning Li
Xiaoyue Li
Jian Zhou
Li’ang Yu
Shufen Li
Yulan Zhang
Ruiyun Qin
Wujun Gao
Chuanliang Deng
Genome-Wide Analysis of Transposable Elements and Satellite DNAs in Spinacia Species to Shed Light on Their Roles in Sex Chromosome Evolution
Frontiers in Plant Science
repetitive DNA sequences
rDNA
homomorphic sex chromosome
heteromorphic sex chromosome
long terminal repeat retroelements
next generation sequencing
author_facet Ning Li
Xiaoyue Li
Jian Zhou
Li’ang Yu
Shufen Li
Yulan Zhang
Ruiyun Qin
Wujun Gao
Chuanliang Deng
author_sort Ning Li
title Genome-Wide Analysis of Transposable Elements and Satellite DNAs in Spinacia Species to Shed Light on Their Roles in Sex Chromosome Evolution
title_short Genome-Wide Analysis of Transposable Elements and Satellite DNAs in Spinacia Species to Shed Light on Their Roles in Sex Chromosome Evolution
title_full Genome-Wide Analysis of Transposable Elements and Satellite DNAs in Spinacia Species to Shed Light on Their Roles in Sex Chromosome Evolution
title_fullStr Genome-Wide Analysis of Transposable Elements and Satellite DNAs in Spinacia Species to Shed Light on Their Roles in Sex Chromosome Evolution
title_full_unstemmed Genome-Wide Analysis of Transposable Elements and Satellite DNAs in Spinacia Species to Shed Light on Their Roles in Sex Chromosome Evolution
title_sort genome-wide analysis of transposable elements and satellite dnas in spinacia species to shed light on their roles in sex chromosome evolution
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-01-01
description Sex chromosome evolution has mostly been studied in species with heteromorphic sex chromosomes. The Spinacia genus serves as an ideal model for investigating evolutionary mechanisms underlying the transition from homomorphic to heteromorphic sex chromosomes. Among evolutionary factors, repetitive sequences play multiple roles in sex chromosome evolution while their forces have not been fully explored in Spinacia species. Here, we identified major repetitive sequence classes in male and female genomes of Spinacia species and their ancestral relative sugar beet to elucidate the evolutionary processes of sex chromosome evolution using next-generation sequencing (NGS) data. Comparative analysis revealed that the repeat elements of Spinacia species are considerably higher than of sugar beet, especially the Ty3/Gypsy and Ty1/Copia retrotransposons. The long terminal repeat retroelements (LTR) Angela, Athila, and Ogre may be accounted for the higher proportion of repeats in the spinach genome. Comparison of the repeats proportion between female and male genomes of three Spinacia species indicated the different representation in Spinacia tetrandra samples but not in the S. oleracea or S. turkestanica samples. From these results, we speculated that emergence of repetitive DNA sequences may correlate the formation of sex chromosome and the transition from homomorphic sex chromosomes to heteromorphic sex chromosomes as heteromorphic sex chromosomes exclusively existed in Spinacia tetrandra. Three novel sugar beet-specific satellites were identified and confirmed by fluorescence in situ hybridization (FISH); six out of eight new spinach-specific satellites were mapped to the short arm of sex chromosomes. A total of 141 copies of SolSat01-171-s were found in the sex determination region (SDR). Thus, the accumulation of satellite DNA on the short arm of chromosome 1 may be involved in the sex chromosome evolution in Spinacia species. Our study provides a fundamental resource for understanding repeat sequences in Spinacia species and their roles in sex chromosome evolution.
topic repetitive DNA sequences
rDNA
homomorphic sex chromosome
heteromorphic sex chromosome
long terminal repeat retroelements
next generation sequencing
url https://www.frontiersin.org/articles/10.3389/fpls.2020.575462/full
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