Phased Assembly of Neo-Sex Chromosomes Reveals Extensive Y
Degeneration and Rapid Genome Evolution in Rumex hastatulus

J 2024

Phased Assembly of Neo-Sex Chromosomes Reveals Extensive Y Degeneration and Rapid Genome Evolution in Rumex hastatulus

SACCHI, Bianca, Zoë HUMPHRIES, Jana KRUŽLICOVÁ, Markéta BODLÁKOVÁ, Cassandre PYNE et. al.

Basic information

Original name

Phased Assembly of Neo-Sex Chromosomes Reveals Extensive Y Degeneration and Rapid Genome Evolution in Rumex hastatulus

Authors

SACCHI, Bianca, Zoë HUMPHRIES, Jana KRUŽLICOVÁ (703 Slovakia, belonging to the institution), Markéta BODLÁKOVÁ, Cassandre PYNE, Baharul I CHOUDHURY, Yunchen GONG, Václav BAČOVSKÝ, Roman HOBZA, Spencer C H BARRETT and Stephen I WRIGHT

Edition

Molecular Biology and Evolution, Oxford University Press, 2024, 0737-4038

Other information

Language

English

Type of outcome

Článek v odborném periodiku

Field of Study

10608 Biochemistry and molecular biology

Country of publisher

United Kingdom of Great Britain and Northern Ireland

Confidentiality degree

není předmětem státního či obchodního tajemství

References:

URL

Impact factor

Impact factor: 10.700 in 2022

Organization unit

Faculty of Science

DOI

http://dx.doi.org/10.1093/molbev/msae074

UT WoS

001209445000001

Keywords in English

sex chromosomes; plants; genomics; transposable elements

Abstract

V originále

Y chromosomes are thought to undergo progressive degeneration due to stepwise loss of recombination and subsequent reduction in selection efficiency. However, the timescales and evolutionary forces driving degeneration remain unclear. To investigate the evolution of sex chromosomes on multiple timescales, we generated a high-quality phased genome assembly of the massive older (<10 MYA) and neo (<200,000 yr) sex chromosomes in the XYY cytotype of the dioecious plant Rumex hastatulus and a hermaphroditic outgroup Rumex salicifolius. Our assemblies, supported by fluorescence in situ hybridization, confirmed that the neo-sex chromosomes were formed by two key events: an X-autosome fusion and a reciprocal translocation between the homologous autosome and the Y chromosome. The enormous sex-linked regions of the X (296 Mb) and two Y chromosomes (503 Mb) both evolved from large repeat-rich genomic regions with low recombination; however, the complete loss of recombination on the Y still led to over 30% gene loss and major rearrangements. In the older sex-linked region, there has been a significant increase in transposable element abundance, even into and near genes. In the neo-sex-linked regions, we observed evidence of extensive rearrangements without gene degeneration and loss. Overall, we inferred significant degeneration during the first 10 million years of Y chromosome evolution but not on very short timescales. Our results indicate that even when sex chromosomes emerge from repetitive regions of already-low recombination, the complete loss of recombination on the Y chromosome still leads to a substantial increase in repetitive element content and gene degeneration.

Citovat

SACCHI, Bianca, Zoë HUMPHRIES, Jana KRUŽLICOVÁ, Markéta BODLÁKOVÁ, Cassandre PYNE, Baharul I CHOUDHURY, Yunchen GONG, Václav BAČOVSKÝ, Roman HOBZA, Spencer C H BARRETT and Stephen I WRIGHT. Phased Assembly of Neo-Sex Chromosomes Reveals Extensive Y Degeneration and Rapid Genome Evolution in Rumex hastatulus. Molecular Biology and Evolution. Oxford University Press, 2024, vol. 41, No 4, p. 1-15. ISSN 0737-4038. Available from: https://dx.doi.org/10.1093/molbev/msae074.

@article{2400319,
   author = {Sacchi, Bianca and Humphries, Zoë and Kružlicová, Jana and Bodláková, Markéta and Pyne, Cassandre and Choudhury, Baharul I and Gong, Yunchen and Bačovský, Václav and Hobza, Roman and Barrett, Spencer C H and Wright, Stephen I},
   article_number = {4},
   doi = {http://dx.doi.org/10.1093/molbev/msae074},
   keywords = {sex chromosomes; plants; genomics; transposable elements},
   language = {eng},
   issn = {0737-4038},
   journal = {Molecular Biology and Evolution},
   title = {Phased Assembly of Neo-Sex Chromosomes Reveals Extensive Y Degeneration and Rapid Genome Evolution in Rumex hastatulus},
   url = {https://academic.oup.com/mbe/article/41/4/msae074/7644656},
   volume = {41},
   year = {2024}
}

TY  - JOUR
ID  - 2400319
AU  - Sacchi, Bianca - Humphries, Zoë - Kružlicová, Jana - Bodláková, Markéta - Pyne, Cassandre - Choudhury, Baharul I - Gong, Yunchen - Bačovský, Václav - Hobza, Roman - Barrett, Spencer C H - Wright, Stephen I
PY  - 2024
TI  - Phased Assembly of Neo-Sex Chromosomes Reveals Extensive Y Degeneration and Rapid Genome Evolution in Rumex hastatulus
JF  - Molecular Biology and Evolution
VL  - 41
IS  - 4
SP  - 1-15
EP  - 1-15
PB  - Oxford University Press
SN  - 07374038
KW  - sex chromosomes
KW  - plants
KW  - genomics
KW  - transposable elements
UR  - https://academic.oup.com/mbe/article/41/4/msae074/7644656
N2  - Y chromosomes are thought to undergo progressive degeneration due to stepwise loss of recombination and subsequent reduction in selection efficiency. However, the timescales and evolutionary forces driving degeneration remain unclear. To investigate the evolution of sex chromosomes on multiple timescales, we generated a high-quality phased genome assembly of the massive older (<10 MYA) and neo (<200,000 yr) sex chromosomes in the XYY cytotype of the dioecious plant Rumex hastatulus and a hermaphroditic outgroup Rumex salicifolius. Our assemblies, supported by fluorescence in situ hybridization, confirmed that the neo-sex chromosomes were formed by two key events: an X-autosome fusion and a reciprocal translocation between the homologous autosome and the Y chromosome. The enormous sex-linked regions of the X (296 Mb) and two Y chromosomes (503 Mb) both evolved from large repeat-rich genomic regions with low recombination; however, the complete loss of recombination on the Y still led to over 30% gene loss and major rearrangements. In the older sex-linked region, there has been a significant increase in transposable element abundance, even into and near genes. In the neo-sex-linked regions, we observed evidence of extensive rearrangements without gene degeneration and loss. Overall, we inferred significant degeneration during the first 10 million years of Y chromosome evolution but not on very short timescales. Our results indicate that even when sex chromosomes emerge from repetitive regions of already-low recombination, the complete loss of recombination on the Y chromosome still leads to a substantial increase in repetitive element content and gene degeneration.
ER  -

SACCHI, Bianca, Zo$\backslash$''e HUMPHRIES, Jana KRUŽLICOVÁ, Markéta BODLÁKOVÁ, Cassandre PYNE, Baharul I CHOUDHURY, Yunchen GONG, Václav BAČOVSKÝ, Roman HOBZA, Spencer C H BARRETT and Stephen I WRIGHT. Phased Assembly of Neo-Sex Chromosomes Reveals Extensive Y Degeneration and Rapid Genome Evolution in Rumex hastatulus. \textit{Molecular Biology and Evolution}. Oxford University Press, 2024, vol.~41, No~4, p.~1-15. ISSN~0737-4038. Available from: https://dx.doi.org/10.1093/molbev/msae074.

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