Evidence for dosage compensation in Silene latifolia, a plant with 10-million-year-old sex chromosomes, reveals that dosage compensation can evolve rapidly in young XY systems and is not an animal-specific phenomenon

A Oshlack

Alex Widmer

Aline Muyle

B Charlesworth

B Vicoso

B. T Lahn

C Delichère

C Desfeux

C Kohler

C Lemaitre

Clothilde Deschamps

D Bachtrog

D Charlesworth

D. A Filatov

D. B Sloan

D. S Guttman

Detlef Weigel

E Kejnovsky

E. H Leder

E. J Pritham

F Veyrunes

G Bernasconi

G Robertson

G. A Marais

G. J Wyckoff

Gabriel A. B. Marais

H Ellegren

H Li

H Skaletsky

I Atanassov

I Marin

J Chow

J Deakin

J Engelstädter

J Mank

J. A Birchler

J. A Marshall Graves

J. B Wolf

J. E Deakin

J. E Mank

J. R Walters

J. T Simpson

L Carrel

L Potrzebowski

M Mrackova

M Nicolas

M Westergaard

M. A DePristo

M. A Wilson

M. T Ross

M. V Chibalina

N Blavet

Niklaus Zemp

Q Zhou

R Bergero

R Ming

R Nielsen

R. C Moore

S Bao

S Qiu

S. P Otto

Sylvain Mousset

T Cermak

T Straub

V Laporte

V. B Kaiser

X Deng

X Huang

X Zha

Y Itoh

English

PubMed

Silene latifolia is a dioecious plant with heteromorphic sex chromosomes that have originated only similar to 10 million years ago and is a promising model organism to study sex chromosome evolution in plants. Previous work suggests that S. latifolia XY chromosomes have gradually stopped recombining and the Y chromosome is undergoing degeneration as in animal sex chromosomes. However, this work has been limited by the paucity of sex-linked genes available. Here, we used 35 Gb of RNA-seq data from multiple males (XY) and females (XX) of an S. latifolia inbred line to detect sex-linked SNPs and identified more than 1,700 sex-linked contigs (with X-linked and Y-linked alleles). Analyses using known sex-linked and autosomal genes, together with simulations indicate that these newly identified sex-linked contigs are reliable. Using read numbers, we then estimated expression levels of X-linked and Y-linked alleles in males and found an overall trend of reduced expression of Y-linked alleles, consistent with a widespread ongoing degeneration of the S. latifolia Y chromosome. By comparing expression intensities of X-linked alleles in males and females, we found that X-linked allele expression increases as Y-linked allele expression decreases in males, which makes expression of sex-linked contigs similar in both sexes. This phenomenon is known as dosage compensation and has so far only been observed in evolutionary old animal sex chromosome systems. Our results suggest that dosage compensation has evolved in plants and that it can quickly evolve de novo after the origin of sex chromosomes

Muyle, A.

Zemp, N.

Deschamps, C.

Mousset, Sylvain

Wildmer, A.

Marais, Gabriel

Hal-Diderot

Rapid De Novo Evolution of X Chromosome Dosage Compensation in Silene latifolia a Plant with Young Sex Chromosomes

Muyle Aline

Zemp Niklaus

Deschamps Clothilde

Mousset Sylvain

Widmer Alex

Marais Gabriel A. B.

Public Library of Science (PLOS)

, a Plant with Young Sex Chromosomes

Silene latifolia is a dioecious plant with heteromorphic sex chromosomes that have originated only ∼10 million years ago and is a promising model organism to study sex chromosome evolution in plants. Previous work suggests that S. latifolia XY chromosomes have gradually stopped recombining and the Y chromosome is undergoing degeneration as in animal sex chromosomes. However, this work has been limited by the paucity of sex-linked genes available. Here, we used 35 Gb of RNA-seq data from multiple males (XY) and females (XX) of an S. latifolia inbred line to detect sex-linked SNPs and identified more than 1,700 sex-linked contigs (with X-linked and Y-linked alleles). Analyses using known sex-linked and autosomal genes, together with simulations indicate that these newly identified sex-linked contigs are reliable. Using read numbers, we then estimated expression levels of X-linked and Y-linked alleles in males and found an overall trend of reduced expression of Y-linked alleles, consistent with a widespread ongoing degeneration of the S. latifolia Y chromosome. By comparing expression intensities of X-linked alleles in males and females, we found that X-linked allele expression increases as Y-linked allele expression decreases in males, which makes expression of sex-linked contigs similar in both sexes. This phenomenon is known as dosage compensation and has so far only been observed in evolutionary old animal sex chromosome systems. Our results suggest that dosage compensation has evolved in plants and that it can quickly evolve de novo after the origin of sex chromosomes

Gabriel A B Marais

Directory of Open Access Journals

PLoS Biology

Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes.

<div>Silene latifolia is a dioecious plant with heteromorphic sex chromosomes that have originated only ∼10 million years ago and is a promising model organism to study sex chromosome evolution in plants. Previous work suggests that S. latifolia XY chromosomes have gradually stopped recombining and the Y chromosome is undergoing degeneration as in animal sex chromosomes. However, this work has been limited by the paucity of sex-linked genes available. Here, we used 35 Gb of RNA-seq data from multiple males (XY) and females (XX) of an S. latifolia inbred line to detect sex-linked SNPs and identified more than 1,700 sex-linked contigs (with X-linked and Y-linked alleles). Analyses using known sex-linked and autosomal genes, together with simulations indicate that these newly identified sex-linked contigs are reliable. Using read numbers, we then estimated expression levels of X-linked and Y-linked alleles in males and found an overall trend of reduced expression of Y-linked alleles, consistent with a widespread ongoing degeneration of the S. latifolia Y chromosome. By comparing expression intensities of X-linked alleles in males and females, we found that X-linked allele expression increases as Y-linked allele expression decreases in males, which makes expression of sex-linked contigs similar in both sexes. This phenomenon is known as dosage compensation and has so far only been observed in evolutionary old animal sex chromosome systems. Our results suggest that dosage compensation has evolved in plants and that it can quickly evolve de novo after the origin of sex chromosomes. </div

Aline Muyle (170655)

Niklaus Zemp (170658)

Clothilde Deschamps (170662)

Sylvain Mousset (170664)

Alex Widmer (90923)

Gabriel A. B. Marais (170666)

The Francis Crick Institute

Rapid De Novo Evolution of X Chromosome Dosage Compensation in Silene latifolia, a Plant with Young Sex Chromosomes

Silene latifolia is a dioecious plant with heteromorphic sex chromosomes that have originated only ∼10 million years ago and is a promising model organism to study sex chromosome evolution in plants. Previous work suggests that S. latifolia XY chromosomes have gradually stopped recombining and the Y chromosome is undergoing degeneration as in animal sex chromosomes. However, this work has been limited by the paucity of sex-linked genes available. Here, we used 35 Gb of RNA-seq data from multiple males (XY) and females (XX) of an S. latifolia inbred line to detect sex-linked SNPs and identified more than 1,700 sex-linked contigs (with X-linked and Y-linked alleles). Analyses using known sex-linked and autosomal genes, together with simulations indicate that these newly identified sex-linked contigs are reliable. Using read numbers, we then estimated expression levels of X-linked and Y-linked alleles in males and found an overall trend of reduced expression of Y-linked alleles, consistent with a widespread ongoing degeneration of the S. latifolia Y chromosome. By comparing expression intensities of X-linked alleles in males and females, we found that X-linked allele expression increases as Y-linked allele expression decreases in males, which makes expression of sex-linked contigs similar in both sexes. This phenomenon is known as dosage compensation and has so far only been observed in evolutionary old animal sex chromosome systems. Our results suggest that dosage compensation has evolved in plants and that it can quickly evolve de novo after the origin of sex chromosomes.ISSN:1544-9173ISSN:1545-788

Muyle, Aline

Zemp, Niklaus

Deschamps, Clothilde

Widmer, Alex

Marais, Gabriel A.B.

Repository for Publications and Research Data

Rapid De Novo Evolution of X Chromosome Dosage Compensation in Silene latifolia, a Plant with Young Sex Chromosomes

Crossref

HAL: Hyper Article en Ligne

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Rapid De Novo Evolution of X Chromosome Dosage Compensation in Silene latifolia, a Plant with Young Sex Chromosomes

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