scholarly journals Early sex-chromosome evolution in the diploid dioecious plant Mercurialis annua

2017 ◽  
Author(s):  
Paris Veltsos ◽  
Kate E. Ridout ◽  
Melissa A. Toups ◽  
Santiago C. González-Martínez ◽  
Aline Muyle ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Gene Loss ◽  
Sex Chromosome ◽  
Sequence Divergence ◽  
Sex Chromosome Evolution ◽  
Dioecious Plant ◽  
Suppressed Recombination ◽  
Mercurialis Annua

AbstractSuppressed recombination around a sex-determining locus allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. Both genetic mapping and exome resequencing of individuals across the species range independently identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about a third of the Y chromosome has ceased recombining, a region containing 568 transcripts and spanning 22.3 cM in the corresponding female map. Patterns of gene expression hint at the possible role of sexually antagonistic selection in having favored suppressed recombination. In total, the genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. There was limited evidence of Y-chromosome degeneration in terms of gene loss and pseudogenization, but sequence divergence between the X and Y copies of many sex-linked genes was higher than between M. annua and its dioecious sister species M. huetii with which it shares a sex-determining region. The Mendelian inheritance of sex in interspecific crosses, combined with the other observed pattern, suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining about one million years ago.Article summaryPlants that evolved separate sexes (dioecy) recently are ideal models for studying the early stages of sex-chromosome evolution. Here, we use karyological, whole genome and transcriptome data to characterize the homomorphic sex chromosomes of the annual dioecious plant Mercurialis annua. Our analysis reveals many typical hallmarks of dioecy and sex-chromosome evolution, including sex-biased gene expression and high X/Y sequence divergence, yet few premature stop codons in Y-linked genes and very little outright gene loss, despite 1/3 of the sex chromosome having ceased recombination in males. Our results confirm that the M. annua species complex is a fertile system for probing early stages in the evolution of sex chromosomes.

scholarly journals Early Sex-Chromosome Evolution in the Diploid Dioecious Plant Mercurialis annua

Genetics ◽  
2019 ◽  
Vol 212 (3) ◽  
pp. 815-835 ◽  
Author(s):  
Paris Veltsos ◽  
Kate E. Ridout ◽  
Melissa A. Toups ◽  
Santiago C. González-Martínez ◽  
Aline Muyle ◽  
...  
Keyword(s):  
Genetic Mapping ◽  
Y Chromosome ◽  
Sex Chromosomes ◽  
Genome Assembly ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
De Novo ◽  
Sex Chromosome Evolution ◽  
Suppressed Recombination ◽  
Mercurialis Annua

Suppressed recombination allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. The genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. Genetic mapping and exome resequencing of individuals across the species range both identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about one-third of the Y chromosome, containing 568 transcripts and spanning 22.3 cM in the corresponding female map, has ceased recombining. Nevertheless, we found limited evidence for Y-chromosome degeneration in terms of gene loss and pseudogenization, and most X- and Y-linked genes appear to have diverged in the period subsequent to speciation between M. annua and its sister species M. huetii, which shares the same sex-determining region. Taken together, our results suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining ∼1 MYA. Patterns of gene expression within the nonrecombining region are consistent with the idea that sexually antagonistic selection may have played a role in favoring suppressed recombination.

scholarly journals YY males of the dioecious plant Mercurialis annua are fully viable but produce largely infertile pollen

2019 ◽  
Author(s):  
Xinji Li ◽  
Paris Veltsos ◽  
Guillaume Cossard ◽  
Jörn Gerchen ◽  
John R. Pannell
Keyword(s):  
X Chromosome ◽  
Male Fertility ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sequence Divergence ◽  
Sex Chromosome Evolution ◽  
Dioecious Plant ◽  
Significant Difference ◽  
Heterogametic Sex ◽  
Mercurialis Annua

SummaryThe suppression of recombination during sex-chromosome evolution is thought to be favoured by linkage between the sex-determining locus and sexually-antagonistic loci, and leads to the degeneration of the chromosome restricted to the heterogametic sex. Despite substantial evidence for genetic degeneration at the sequence level, the phenotypic effects of the earliest stages of sex-chromosome evolution are poorly known. Here, we compare the morphology, viability and fertility between XY and YY individuals produced by crossing seed-producing males in the dioecious plant Mercurialis annua L., which has young sex chromosomes with limited X-Y sequence divergence. We found no significant difference in viability or vegetative morphology between XY and YY males. However, electron microscopy revealed clear differences in pollen anatomy, and YY males were significantly poorer sires in competition with their XY counterparts. Our study suggests either that the X chromosome is required for full male fertility in M. annua, or that male fertility is sensitive to the dosage of relevant Y-linked genes. We discuss the possibility that the maintenance of male-fertility genes on the X chromosome might have been favoured in recent population expansions, which selected for the ability of females to produce pollen in the absence of males.

scholarly journals Genetic and Functional Analysis of DD44, a Sex-Linked Gene From the Dioecious Plant Silene latifolia, Provides Clues to Early Events in Sex Chromosome Evolution

Genetics ◽  
2003 ◽  
Vol 163 (1) ◽  
pp. 321-334 ◽  
Author(s):  
Richard C Moore ◽  
Olga Kozyreva ◽  
Sabine Lebel-Hardenack ◽  
Jiri Siroky ◽  
Roman Hobza ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Silene Latifolia ◽  
Evolutionary Analysis ◽  
Sex Chromosome Evolution ◽  
Dioecious Plant ◽  
Linked Gene ◽  
Recent Emergence

Abstract Silene latifolia is a dioecious plant with heteromorphic sex chromosomes. The sex chromosomes of S. latifolia provide an opportunity to study the early events in sex chromosome evolution because of their relatively recent emergence. In this article, we present the genetic and physical mapping, expression analysis, and molecular evolutionary analysis of a sex-linked gene from S. latifolia, DD44 (Differential Display 44). DD44 is homologous to the oligomycin sensitivity-conferring protein, an essential component of the mitochondrial ATP synthase, and is ubiquitously expressed in both sexes. We have been able to genetically map DD44 to a region of the Y chromosome that is genetically linked to the carpel-suppressing locus. Although we have physically mapped DD44 to the distal end of the long arm of the X chromosome using fluorescence in situ hybridization (FISH), DD44 maps to the opposite arm of the Y chromosome as determined by our genetic map. These data suggest that chromosomal rearrangements have occurred on the Y chromosome, which may have contributed to the genetic isolation of the Y chromosome. We discuss the implications of these results with respect to the structural and functional evolution of the S. latifolia Y chromosome.

scholarly journals A neutral model for the loss of recombination on sex chromosomes

2021 ◽  
Vol 376 (1832) ◽  
pp. 20200096 ◽  
Author(s):  
Daniel L. Jeffries ◽  
Jörn F. Gerchen ◽  
Mathias Scharmann ◽  
John R. Pannell
Keyword(s):  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sequence Divergence ◽  
Theme Issue ◽  
Recombination Rates ◽  
Natural Systems ◽  
Adaptive Processes ◽  
Sexually Antagonistic Selection ◽  
Suppressed Recombination

The loss of recombination between sex chromosomes has occurred repeatedly throughout nature, with important implications for their subsequent evolution. Explanations for this remarkable convergence have generally invoked only adaptive processes (e.g. sexually antagonistic selection); however, there is still little evidence for these hypotheses. Here we propose a model in which recombination on sex chromosomes is lost due to the neutral accumulation of sequence divergence adjacent to (and thus, in linkage disequilibrium with) the sex determiner. Importantly, we include in our model the fact that sequence divergence, in any form, reduces the probability of recombination between any two sequences. Using simulations, we show that, under certain conditions, a region of suppressed recombination arises and expands outwards from the sex-determining locus, under purely neutral processes. Further, we show that the rate and pattern of recombination loss are sensitive to the pre-existing recombination landscape of the genome and to sex differences in recombination rates, with patterns consistent with evolutionary strata emerging under some conditions. We discuss the applicability of these results to natural systems. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.

scholarly journals Y-chromosome haplotypes of varying differentiation to the X are not associated with male fitness in common frogs

2019 ◽  
Author(s):  
Paris Veltsos ◽  
Nicolas Rodrigues ◽  
Tania Studer ◽  
Wen-Juan Ma ◽  
Roberto Sermier ◽  
...  
Keyword(s):  
Sexual Dimorphism ◽  
Y Chromosome ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sex Chromosome Evolution ◽  
Chromosome Differentiation ◽  
Y Chromosomes ◽  
Male Phenotype ◽  
Xx Males

AbstractThe canonical model of sex-chromosome evolution assigns a key role to sexually antagonistic (SA) genes on the arrest of recombination and ensuing degeneration of Y chromosomes. This assumption cannot be tested in organisms with highly differentiated sex chromosomes, such as mammals or birds, owing to the lack of polymorphism. Fixation of SA alleles, furthermore, might be the consequence rather than the cause of recombination arrest. Here we focus on a population of common frogs (Rana temporaria) where XY males with genetically differentiated Y chromosomes (non-recombinant Y haplotypes) coexist with both XY° males with proto-Y chromosomes (only differentiated from X chromosomes in the immediate vicinity of the candidate sex-determining locus Dmrt1) and XX males with undifferentiated sex chromosomes (genetically identical to XX females). Our study shows no effect of sex-chromosome differentiation on male phenotype, mating success or fathering success. Our conclusions rejoin genomic studies that found no differences in gene expression between XY, XY° and XX males. Sexual dimorphism in common frogs seems to result from the differential expression of autosomal genes rather than sex-linked SA genes. Among-male variance in sex-chromosome differentiation is better explained by a polymorphism in the penetrance of alleles at the sex locus, resulting in variable levels of sex reversal (and thus of X-Y recombination in XY females), independent of sex-linked SA genes.Impact SummaryHumans, like other mammals, present highly differentiated sex chromosomes, with a large, gene-rich X chromosome contrasting with a small, gene-poor Y chromosome. This differentiation results from a process that started approximately 160 Mya, when the Y first stopped recombining with the X. How and why this happened, however, remain controversial. According to the canonical model, the process was initiated by sexually antagonistic selection; namely, selection on the proto-Y chromosome for alleles that were beneficial to males but detrimental to females. The arrest of XY recombination then allowed such alleles to be only transmitted to sons, not to daughters. Although appealing and elegant, this model can no longer be tested in mammals, as it requires a sex-chromosome system at an incipient stage of evolution. Here we focus on a frog that displays within-population polymorphism is sex-chromosome differentiation, where XY males with differentiated chromosomes coexist with XX males lacking Y chromosomes. We find no effect of sex-chromosome differentiation on male phenotype or mating success, opposing expectations from the standard model. Sex linked genes do not seem to have a disproportionate effect on sexual dimorphism. From our results, sexually antagonistic genes show no association with sex-chromosome differentiation in frogs, which calls for alternative models of sex-chromosome evolution.

scholarly journals The effects of haploid selection on Y chromosome evolution in two closely related dioecious plants

2018 ◽  
Author(s):  
George Sandler ◽  
Felix E.G. Beaudry ◽  
Spencer C.H. Barrett ◽  
Stephen I. Wright
Keyword(s):  
Gene Expression ◽  
Y Chromosome ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sex Chromosome Evolution ◽  
Y Chromosomes ◽  
Expression Bias ◽  
Haploid Selection ◽  
Plant Sex

AbstractThe evolution of sex chromosomes is usually considered to be driven by sexually antagonistic selection in the diploid phase. However, selection during the haploid gametic phase of the lifecycle has recently received theoretical attention as possibly playing a central role in sex chromosome evolution, especially in plants where gene expression in the haploid phase is extensive. In particular, male-specific haploid selection might favour the linkage of pollen beneficial alleles to male sex determining regions on incipient Y chromosomes. This linkage might then allow such alleles to further specialise for the haploid phase. Purifying haploid selection is also expected to slow the degeneration of Y-linked genes expressed in the haploid phase. Here, we examine the evolution of gene expression in flower buds and pollen of two species of Rumex to test for signatures of haploid selection acting during plant sex chromosome evolution. We find that genes with high ancestral pollen expression bias occur more often on sex chromosomes than autosomes and that genes on the Y chromosome are more likely to become enriched for pollen expression bias. We also find that genes with low expression in pollen are more likely to be lost from the Y chromosome. Our results suggest that sex-specific haploid selection during the gametophytic stage of the lifecycle may be a major contributor to several features of plant sex chromosome evolution.

scholarly journals Recombination landscape dimorphism contributes to sex chromosome evolution in the dioecious plant Rumex hastatulus

2021 ◽  
Author(s):  
Joanna L Rifkin ◽  
Solomiya Hnatovzka ◽  
Meng Yuan ◽  
Bianca M Sacchi ◽  
Baharul I Choudhury ◽  
...  
Keyword(s):  
Sex Differences ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Pollen Competition ◽  
Sex Chromosome Evolution ◽  
Dioecious Plant ◽  
Male Recombination ◽  
Rumex Hastatulus ◽  
Heterogametic Sex

There is growing evidence across diverse taxa for sex differences in the genomic landscape of recombination, but the causes and consequences of these differences remain poorly understood. Strong recombination landscape dimorphism between the sexes could have important implications for the dynamics of sex chromosome evolution and turnover because low recombination in the heterogametic sex can help favour the spread of sexually antagonistic alleles. Here, we present a sex-specific linkage map and revised genome assembly of Rumex hastatulus, representing the first characterization of sex differences in recombination landscape in a dioecious plant. We provide evidence for strong sex differences in recombination, with pericentromeric regions of highly suppressed recombination in males that cover over half of the genome. These differences are found on autosomes as well as sex chromosomes, suggesting that pre-existing differences in recombination may have contributed to sex chromosome formation and divergence. Analysis of segregation distortion suggests that haploid selection due to pollen competition occurs disproportionately in regions with low male recombination. Our results are consistent with the hypothesis that sex differences in the recombination landscape contributed to the formation of a large heteromorphic pair of sex chromosomes, and that pollen competition is an important determinant of recombination dimorphism.

scholarly journals Differences in Homomorphic Sex Chromosomes Are Associated with Population Divergence in Sex Determination in Carinascincus ocellatus (Scincidae: Lygosominae)

Cells ◽  
2021 ◽  
Vol 10 (2) ◽  
pp. 291
Author(s):  
Peta Hill ◽  
Foyez Shams ◽  
Christopher P. Burridge ◽  
Erik Wapstra ◽  
Tariq Ezaz
Keyword(s):  
Sex Determination ◽  
Y Chromosome ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Population Divergence ◽  
Sex Chromosome Evolution ◽  
Evolutionary Transitions ◽  
Evolutionary Origins ◽  
Probe Set

Sex determination directs development as male or female in sexually reproducing organisms. Evolutionary transitions in sex determination have occurred frequently, suggesting simple mechanisms behind the transitions, yet their detail remains elusive. Here we explore the links between mechanisms of transitions in sex determination and sex chromosome evolution at both recent and deeper temporal scales (<1 Myr; ~79 Myr). We studied a rare example of a species with intraspecific variation in sex determination, Carinascincus ocellatus, and a relative, Liopholis whitii, using c-banding and mapping of repeat motifs and a custom Y chromosome probe set to identify the sex chromosomes. We identified both unique and conserved regions of the Y chromosome among C. ocellatus populations differing in sex determination. There was no evidence for homology of sex chromosomes between C. ocellatus and L. whitii, suggesting independent evolutionary origins. We discuss sex chromosome homology between members of the subfamily Lygosominae and propose links between sex chromosome evolution, sex determination transitions, and karyotype evolution.

scholarly journals Phylogeny, transposable element and sex chromosome evolution of the basal lineage of birds

2019 ◽  
Author(s):  
Zongji Wang ◽  
Jilin Zhang ◽  
Xiaoman Xu ◽  
Christopher Witt ◽  
Yuan Deng ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sequence Divergence ◽  
South American ◽  
Sex Chromosome Evolution ◽  
Rapid Speciation ◽  
Genome Wide ◽  
Divergence Pattern ◽  
Female Specific

AbstractSex chromosomes of mammals and most birds are heteromorphic, while those of many paleognaths (ratites and tinamous) are inexplicably homomorphic. To dissect the mechanisms underlying the different tempo of sex chromosome evolution, we produced high-quality genomes of 12 paleognathous species, and reconstructed their phylogeny based on alignments of the non-coding sequences extending to nearly 40% of the genome. Our phylogenomic tree grouped the South American rheas and tinamous together, and supported the independent evolution of gigantism and loss of flight among ratites. The small-bodied tinamous have much higher rates of genome-wide substitutions and transposon turnovers. Yet majorities of both have retained exceptionally long recombining regions occupying over half of the entire sex chromosome, with the rest sex-linked regions diverging from each other at a much lower rate relative to neognathous birds. Each species exhibits a punctuated sequence divergence pattern between sex chromosomes termed ‘evolutionary strata’, because of stepwise suppression of recombination. We concluded that all paleognaths share one evolutionary stratum with all other birds, and convergently formed between one to three strata after their rapid speciation. Contrary to the classic notion, we provided clear evidence that the youngest stratum of some tinamous formed without chromosomal inversion. Intriguingly, some of the encompassing W-linked genes have upregulated their expression levels in ovary, probably due to the female-specific selection. We proposed here that the unique male-only parental care system of paleognaths has reduced the intensity of sexual selection, and contributed to these species’ low rates of sex chromosome evolution. We also provided novel insights into the evolution of W-linked genes at their early stages.

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