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

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.

2017 ◽  
Author(s):  
Paris Veltsos ◽  
Kate E. Ridout ◽  
Melissa A. Toups ◽  
Santiago C. González-Martínez ◽  
Aline Muyle ◽  
...  

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.


2021 ◽  
Author(s):  
Joanna L Rifkin ◽  
Solomiya Hnatovzka ◽  
Meng Yuan ◽  
Bianca M Sacchi ◽  
Baharul I Choudhury ◽  
...  

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.


CYTOLOGIA ◽  
2010 ◽  
Vol 75 (3) ◽  
pp. 319-325 ◽  
Author(s):  
Rie Nishiyama ◽  
Kotaro Ishii ◽  
Etsuko Kifune ◽  
Yusuke Kazama ◽  
Kiyoshi Nishihara ◽  
...  

2010 ◽  
Vol 27 (7) ◽  
pp. 1495-1503 ◽  
Author(s):  
Erica H. Leder ◽  
Jose M. Cano ◽  
Tuomas Leinonen ◽  
Robert B. O'Hara ◽  
Mikko Nikinmaa ◽  
...  

Genetics ◽  
2003 ◽  
Vol 165 (3) ◽  
pp. 1317-1328 ◽  
Author(s):  
Bryant F McAllister

Abstract Sex chromosomes originate from pairs of autosomes that acquire controlling genes in the sex-determining cascade. Universal mechanisms apparently influence the evolution of sex chromosomes, because this chromosomal pair is characteristically heteromorphic in a broad range of organisms. To examine the pattern of initial differentiation between sex chromosomes, sequence analyses were performed on a pair of newly formed sex chromosomes in Drosophila americana. This species has neo-sex chromosomes as a result of a centromeric fusion between the X chromosome and an autosome. Sequences were analyzed from the Alcohol dehydrogenase (Adh), big brain (bib), and timeless (tim) gene regions, which represent separate positions along this pair of neo-sex chromosomes. In the northwestern range of the species, the bib and Adh regions exhibit significant sequence differentiation for neo-X chromosomes relative to neo-Y chromosomes from the same geographic region and other chromosomal populations of D. americana. Furthermore, a nucleotide site defining a common haplotype in bib is shown to be associated with a paracentric inversion [In(4)ab] on the neo-X chromosome, and this inversion suppresses recombination between neo-X and neo-Y chromosomes. These observations are consistent with the inversion acting as a recombination modifier that suppresses exchange between these neo-sex chromosomes, as predicted by models of sex chromosome evolution.


2020 ◽  
Vol 12 (6) ◽  
pp. 750-763 ◽  
Author(s):  
Benjamin L S Furman ◽  
David C H Metzger ◽  
Iulia Darolti ◽  
Alison E Wright ◽  
Benjamin A Sandkam ◽  
...  

Abstract Genomic analysis of many nonmodel species has uncovered an incredible diversity of sex chromosome systems, making it possible to empirically test the rich body of evolutionary theory that describes each stage of sex chromosome evolution. Classic theory predicts that sex chromosomes originate from a pair of homologous autosomes and recombination between them is suppressed via inversions to resolve sexual conflict. The resulting degradation of the Y chromosome gene content creates the need for dosage compensation in the heterogametic sex. Sex chromosome theory also implies a linear process, starting from sex chromosome origin and progressing to heteromorphism. Despite many convergent genomic patterns exhibited by independently evolved sex chromosome systems, and many case studies supporting these theoretical predictions, emerging data provide numerous interesting exceptions to these long-standing theories, and suggest that the remarkable diversity of sex chromosomes is matched by a similar diversity in their evolution. For example, it is clear that sex chromosome pairs are not always derived from homologous autosomes. In addition, both the cause and the mechanism of recombination suppression between sex chromosome pairs remain unclear, and it may be that the spread of recombination suppression is a more gradual process than previously thought. It is also clear that dosage compensation can be achieved in many ways, and displays a range of efficacy in different systems. Finally, the remarkable turnover of sex chromosomes in many systems, as well as variation in the rate of sex chromosome divergence, suggest that assumptions about the inevitable linearity of sex chromosome evolution are not always empirically supported, and the drivers of the birth–death cycle of sex chromosome evolution remain to be elucidated. Here, we concentrate on how the diversity in sex chromosomes across taxa highlights an equal diversity in each stage of sex chromosome evolution.


2019 ◽  
Author(s):  
Zongji Wang ◽  
Jilin Zhang ◽  
Xiaoman Xu ◽  
Christopher Witt ◽  
Yuan Deng ◽  
...  

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.


BMC Biology ◽  
2019 ◽  
Vol 17 (1) ◽  
Author(s):  
Richard P. Meisel ◽  
Pablo J. Delclos ◽  
Judith R. Wexler

Abstract Background Sex chromosome evolution is a dynamic process that can proceed at varying rates across lineages. For example, different chromosomes can be sex-linked between closely related species, whereas other sex chromosomes have been conserved for > 100 million years. Cases of long-term sex chromosome conservation could be informative of factors that constrain sex chromosome evolution. Cytological similarities between the X chromosomes of the German cockroach (Blattella germanica) and most flies suggest that they may be homologous—possibly representing an extreme case of long-term conservation. Results To test the hypothesis that the cockroach and fly X chromosomes are homologous, we analyzed whole-genome sequence data from cockroaches. We found evidence in both sequencing coverage and heterozygosity that a significant excess of the same genes are on both the cockroach and fly X chromosomes. We also present evidence that the candidate X-linked cockroach genes may be dosage compensated in hemizygous males. Consistent with this hypothesis, three regulators of transcription and chromatin on the fly X chromosome are conserved in the cockroach genome. Conclusions Our results support our hypothesis that the German cockroach shares the same X chromosome as most flies. This may represent the convergent evolution of the X chromosome in the lineages leading to cockroaches and flies. Alternatively, the common ancestor of most insects may have had an X chromosome that resembled the extant cockroach and fly X. Cockroaches and flies diverged ∼ 400 million years ago, which would be the longest documented conservation of a sex chromosome. Cockroaches and flies have different mechanisms of sex determination, raising the possibility that the X chromosome was conserved despite the evolution of the sex determination pathway.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Juan Liu ◽  
Jennifer Han ◽  
Anupma Sharma ◽  
Ching Man Wai ◽  
Ray Ming ◽  
...  

AbstractSex chromosome evolution results in the disparity in gene content between heterogametic sex chromosomes and creates the need for dosage compensation to counteract the effects of gene dose imbalance of sex chromosomes in males and females. It is not known at which stage of sex chromosome evolution dosage compensation would evolve. We used global gene expression profiling in male and female papayas to assess gene expression patterns of sex-linked genes on the papaya sex chromosomes. By analyzing expression ratios of sex-linked genes to autosomal genes and sex-linked genes in males relative to females, our results showed that dosage compensation was regulated on a gene-by-gene level rather than whole sex-linked region in papaya. Seven genes on the papaya X chromosome exhibited dosage compensation. We further compared gene expression ratios in the two evolutionary strata. Y alleles in the older evolutionary stratum showed reduced expression compared to X alleles, while Y alleles in the younger evolutionary stratum showed elevated expression compared to X alleles. Reduced expression of Y alleles in the older evolutionary stratum might be caused by accumulation of deleterious mutations in regulatory regions or transposable element-mediated methylation spreading. Most X-hemizygous genes exhibited either no or very low expression, suggesting that gene silencing might play a role in maintaining transcriptional balance between females and males.


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