Plant sex chromosomes defy evolutionary models of expanding recombination suppression and genetic degeneration

Renner, Susanne S.; Müller, Niels A.

doi:10.1038/s41477-021-00884-3

Cited by 74 publications

(113 citation statements)

References 107 publications

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“…Undoubtedly sex chromosomes have been less intensively studied in plants, yet there seem to be fundamental differences in the evolution of sex chromosomes in plants and animals (e.g. lack of strong sexual dimorphism in plants, discussed in Renner & Müller, 2021). However, the extent of the differences needs to be clarified and more plant sex chromosomes need to be studied.…”

Section: Introductionmentioning

confidence: 99%

“…Prentout et al ., 2020). Moreover, some systems do not a evolve large nonrecombining region and stay homomorphic (Renner & Müller, 2021).…”

Section: Introductionmentioning

confidence: 99%

“…A few cases in which dioecy evolved longer ago also exist (Käfer et al ., 2017), but no strongly degenerated sex chromosomes have been described so far (Renner & Muller, 2021). Pucholt et al , (2017) described very young sex chromosomes in Salix viminalis despite ancestral dioecy for the sister genera Salix and Populus .…”

Section: Introductionmentioning

confidence: 99%

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Plant genera Cannabis and Humulus share the same pair of well‐differentiated sex chromosomes

et al. 2021

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We recently described, in Cannabis sativa, the oldest sex chromosome system documented so far in plants (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28). Based on the estimated age, we predicted that it should be shared by its sister genus Humulus, which is known also to possess XY chromosomes.Here, we used transcriptome sequencing of an F 1 family of H. lupulus to identify and study the sex chromosomes in this species using the probabilistic method SEX-DETECTOR.We identified 265 sex-linked genes in H. lupulus, which preferentially mapped to the C. sativa X chromosome. Using phylogenies of sex-linked genes, we showed that a region of the sex chromosomes had already stopped recombining in an ancestor of both species. Furthermore, as in C. sativa, Y-linked gene expression reduction is correlated to the position on the X chromosome, and highly Y degenerated genes showed dosage compensation.We report, for the first time in Angiosperms, a sex chromosome system that is shared by two different genera. Thus, recombination suppression started at least 21-25 Myr ago, and then (either gradually or step-wise) spread to a large part of the sex chromosomes (c. 70%), leading to a degenerated Y chromosome.

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Section: Introductionmentioning

confidence: 99%

“…Prentout et al ., 2020). Moreover, some systems do not a evolve large nonrecombining region and stay homomorphic (Renner & Müller, 2021).…”

Section: Introductionmentioning

confidence: 99%

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Plant genera Cannabis and Humulus share the same pair of well‐differentiated sex chromosomes

et al. 2021

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“…These could still be in the initial stages of degeneration as is the situation in wild strawberry [ 8 , 9 ], garden asparagus [ 10 ] and papaya [ 11 , 12 ]. However, in a recent review, based on empirical data, it was shown that the size of the sex determining region was not correlated with age indicating that the theory predicting homomorphic sex chromosomes to be in an early evolutionary stage does not hold [ 13 ]. In some clades, closely related species have different SD loci due to rapid and repeated turnover of sex chromosomes across short evolutionary timescales [ 14 – 16 ].…”

Section: Introductionmentioning

confidence: 99%

Genome-wide association mapping uncovers sex-associated copy number variation markers and female hemizygous regions on the W chromosome in Salix viminalis

et al. 2021

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Background Sex chromosomes are in some species largely undifferentiated (homomorphic) with restricted sex determination regions. Homomorphic but different sex chromosomes are found in the closely related genera Populus and Salix indicating flexible sex determination systems, ideal for studies of processes involved in sex chromosome evolution. We have performed genome-wide association studies of sex and analysed sex chromosomes in a population of 265 wild collected Salix viminalis accessions and studied the sex determining locus. Results A total of 19,592 markers were used in association analyses using both Fisher’s exact tests and a single-marker mixed linear model, which resulted in 48 and 41 sex-associated (SA) markers respectively. Across all 48 SA markers, females were much more often heterozygous than males, which is expected if females were the heterogametic sex. The majority of the SA markers were, based on positions in the S. purpurea genome, located on chromosome 15, previously demonstrated to be the sex chromosome. Interestingly, when mapping the genotyping-by-sequencing sequence tag harbouring the two SA markers with the highest significance to the S. viminalis genomic scaffolds, five regions of very high similarity were found: three on a scaffold that represents a part of chromosome 15, one on a scaffold that represents a part of chromosome 9 and one on a scaffold not anchored to the genome. Based on segregation differences of the alleles at the two marker positions and on differences in PCR amplification between females and males we conclude that females had multiple copies of this DNA fragment (chromosome 9 and 15), whereas males only had one (chromosome 9). We therefore postulate that the female specific sequences have been copied from chromosome 9 and inserted on chromosome 15, subsequently developing into a hemizygous W chromosome linked region. Conclusions Our results support that sex determination in S. viminalis is controlled by one locus on chromosome 15. The segregation patterns observed at the SA markers furthermore confirm that S. viminalis females are the heterogametic sex. We also identified a translocation from chromosome 9 to the W chromosome.

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“…Many Drosophila possess neo-sex chromosomes, but only some of those neo-Ys have degenerated ( Vicoso and Bachtrog 2015 ). Finally, most dioecious plants have homomorphic sex chromosomes with small SDRs ( Renner and Muller 2021 ), but the Y chromosome of some (e.g., Silene latifolia and Rumex hastatulus ) have degenerated extensively ( Papadopulos et al 2015 ).…”

Section: Introductionmentioning

confidence: 99%

Heterogeneous Histories of Recombination Suppression on Stickleback Sex Chromosomes

Sardell

Josephson

Dalziel

et al. 2021

Molecular Biology and Evolution

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How consistent are the evolutionary trajectories of sex chromosomes shortly after they form? Insights into the evolution of recombination, differentiation, and degeneration can be provided by comparing closely related species with homologous sex chromosomes. The sex chromosomes of the threespine stickleback (Gasterosteus aculeatus) and its sister species, the Japan Sea stickleback (G. nipponicus), have been well characterized. Little is known, however, about the sex chromosomes of their congener, the blackspotted stickleback (G. wheatlandi). We used pedigrees to obtain experimentally phased whole genome sequences from blackspotted stickleback X and Y chromosomes. Using multispecies gene trees and analysis of shared duplications, we demonstrate that Chromosome 19 is the ancestral sex chromosome and that its oldest stratum evolved in the common ancestor of the genus. After the blackspotted lineage diverged, its sex chromosomes experienced independent and more extensive recombination suppression, greater X-Y differentiation, and a much higher rate of Y degeneration than the other two species. These patterns may result from a smaller effective population size in the blackspotted stickleback. A recent fusion between the ancestral blackspotted stickleback Y chromosome and Chromosome 12, which produced a neo-X and neo-Y, may have been favored by the very small size of the recombining region on the ancestral sex chromosome. We identify six strata on the ancestral and neo-sex chromosomes where recombination between the X and Y ceased at different times. These results confirm that sex chromosomes can evolve large differences within and between species over short evolutionary timescales.

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Plant sex chromosomes defy evolutionary models of expanding recombination suppression and genetic degeneration

Cited by 74 publications

References 107 publications

Plant genera Cannabis and Humulus share the same pair of well‐differentiated sex chromosomes

Plant genera Cannabis and Humulus share the same pair of well‐differentiated sex chromosomes

Genome-wide association mapping uncovers sex-associated copy number variation markers and female hemizygous regions on the W chromosome in Salix viminalis

Heterogeneous Histories of Recombination Suppression on Stickleback Sex Chromosomes

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