Histone post-translational modifications in Silene latifolia X and Y chromosomes suggest a mammal-like dosage compensation system

Plant Science ◽  
2020 ◽  
Vol 299 ◽  
pp. 110528
Author(s):  
José Luis Rodríguez Lorenzo ◽  
Marcel Hubinský ◽  
Boris Vyskot ◽  
Roman Hobza
Keyword(s):  
Dosage Compensation ◽  
Compensation System ◽  
Silene Latifolia ◽  
Post Translational Modifications ◽  
Y Chromosomes

scholarly journals Genomic imprinting mediates dosage compensation in a young plant XY system

2017 ◽  
Author(s):  
Aline Muyle ◽  
Niklaus Zemp ◽  
Cécile Fruchard ◽  
Radim Cegan ◽  
Jan Vrana ◽  
...  
Keyword(s):  
Gene Expression ◽  
Genomic Imprinting ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Evolutionary Biology ◽  
Early Stage ◽  
Silene Latifolia ◽  
Negative Effects ◽  
Y Chromosomes ◽  
Sex Determination System

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100044).Sex chromosomes have repeatedly evolved from a pair of autosomes1. Consequently, X and Y chromosomes initially have similar gene content, but ongoing Y degeneration leads to reduced Y gene expression and eventual Y gene loss. The resulting imbalance in gene expression between Y genes and the rest of the genome is expected to reduce male fitness, especially when protein networks have components from both autosomes and sex chromosomes. A diverse set of dosage compensating mechanisms that alleviates these negative effects has been described in animals2–4. However, the early steps in the evolution of dosage compensation remain unknown and dosage compensation is poorly understood in plants5. Here we show a novel dosage compensation mechanism in the evolutionarily young XY sex determination system of the plant Silene latifolia. Genomic imprinting results in higher expression from the maternal X chromosome in both males and females. This compensates for reduced Y expression in males but results in X overexpression in females and may be detrimental. It could represent a transient early stage in the evolution of dosage compensation. Our finding has striking resemblance to the first stage proposed by Ohno for the evolution of X inactivation in mammals.

scholarly journals Evidence for dosage compensation in Coccinia grandis, a plant with a highly heteromorphic XY system

2020 ◽  
Author(s):  
Cécile Fruchard ◽  
Hélène Badouin ◽  
David Latrasse ◽  
Ravi S. Devani ◽  
Aline Muyle ◽  
...  
Keyword(s):  
Dosage Compensation ◽  
Gene Loss ◽  
Silene Latifolia ◽  
Plant Family ◽  
Rna Sequences ◽  
Expression Ratio ◽  
Coccinia Grandis ◽  
Y Chromosomes ◽  
Elevated Expression ◽  
Y Degeneration

AbstractSome ~15.000 angiosperms are dioecious, but mechanisms of sex determination in plants remain poorly understood. In particular, how Y chromosomes evolve and degenerate, and whether dosage compensation evolves as a response, are matters of debate. Here we focus on Coccinia grandis, a dioecious cucurbit with the highest level of X/Y heteromorphy recorded so far. We identified sex-linked genes using RNA sequences from a cross and a model-based method termed SEX-DETector. Parents and F1 individuals were genotyped and the transmission patterns of SNPs then analysed. In the >1300 sex-linked genes studied, X-Y divergence was 0.13 - 0.17, and substantial Y degeneration is implied by an average Y/X expression ratio of 0.63 and an inferred gene loss on the Y of ~40%. We also found reduced Y gene expression being compensated by elevated expression of corresponding genes on the X and an excess of sex-biased genes on the sex chromosomes. Molecular evolution of sex-linked genes in C. grandis is thus comparable to that in Silene latifolia, another dioecious plant with a strongly heteromorphic XY system, and cucurbits are the fourth plant family in which dosage compensation is described, suggesting it might be common in plants.

scholarly journals Evidence for Dosage Compensation in Coccinia grandis, a Plant with a Highly Heteromorphic XY System

Genes ◽  
2020 ◽  
Vol 11 (7) ◽  
pp. 787
Author(s):  
Cécile Fruchard ◽  
Hélène Badouin ◽  
David Latrasse ◽  
Ravi S. Devani ◽  
Aline Muyle ◽  
...  
Keyword(s):  
Dosage Compensation ◽  
Gene Loss ◽  
Silene Latifolia ◽  
Plant Family ◽  
Rna Sequences ◽  
Expression Ratio ◽  
Coccinia Grandis ◽  
Y Chromosomes ◽  
Elevated Expression ◽  
Y Degeneration

About 15,000 angiosperms are dioecious, but the mechanisms of sex determination in plants remain poorly understood. In particular, how Y chromosomes evolve and degenerate, and whether dosage compensation evolves as a response, are matters of debate. Here, we focus on Coccinia grandis, a dioecious cucurbit with the highest level of X/Y heteromorphy recorded so far. We identified sex-linked genes using RNA sequences from a cross and a model-based method termed SEX-DETector. Parents and F1 individuals were genotyped, and the transmission patterns of SNPs were then analyzed. In the >1300 sex-linked genes studied, maximum X-Y divergence was 0.13–0.17, and substantial Y degeneration is implied by an average Y/X expression ratio of 0.63 and an inferred gene loss on the Y of ~40%. We also found reduced Y gene expression being compensated by elevated expression of corresponding genes on the X and an excess of sex-biased genes on the sex chromosomes. Molecular evolution of sex-linked genes in C. grandis is thus comparable to that in Silene latifolia, another dioecious plant with a strongly heteromorphic XY system, and cucurbits are the fourth plant family in which dosage compensation is described, suggesting it might be common in plants.

scholarly journals Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

2019 ◽  
Vol 116 (38) ◽  
pp. 19031-19036 ◽  
Author(s):  
Iulia Darolti ◽  
Alison E. Wright ◽  
Benjamin A. Sandkam ◽  
Jake Morris ◽  
Natasha I. Bloch ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Poecilia Reticulata ◽  
Sex Chromosome ◽  
Sequencing Data ◽  
Chromosome Differentiation ◽  
Y Chromosomes ◽  
Shared Ancestry ◽  
Suppressed Recombination

Once recombination is halted between the X and Y chromosomes, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about the variation in sex chromosome differentiation within clades. Here, we combined whole-genome and transcriptome sequencing data to characterize the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged roughly 20 million years ago. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata and P. wingei are largely homomorphic, with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely nonrecombining and strikingly heteromorphic. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of functional chromosome-wide dosage compensation in this species, which has not been previously observed in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

scholarly journals Rapid Y degeneration and dosage compensation in plant sex chromosomes

2015 ◽  
Vol 112 (42) ◽  
pp. 13021-13026 ◽  
Author(s):  
Alexander S. T. Papadopulos ◽  
Michael Chester ◽  
Kate Ridout ◽  
Dmitry A. Filatov
Keyword(s):  
Sex Chromosomes ◽  
Large Scale ◽  
De Novo ◽  
Silene Latifolia ◽  
Stop Codons ◽  
Y Chromosomes ◽  
Evolutionary Trajectories ◽  
Plant Sex Chromosomes ◽  
Two Kingdoms ◽  
Y Degeneration

The nonrecombining regions of animal Y chromosomes are known to undergo genetic degeneration, but previous work has failed to reveal large-scale gene degeneration on plant Y chromosomes. Here, we uncover rapid and extensive degeneration of Y-linked genes in a plant species, Silene latifolia, that evolved sex chromosomes de novo in the last 10 million years. Previous transcriptome-based studies of this species missed unexpressed, degenerate Y-linked genes. To identify sex-linked genes, regardless of their expression, we sequenced male and female genomes of S. latifolia and integrated the genomic contigs with a high-density genetic map. This revealed that 45% of Y-linked genes are not expressed, and 23% are interrupted by premature stop codons. This contrasts with X-linked genes, in which only 1.3% of genes contained stop codons and 4.3% of genes were not expressed in males. Loss of functional Y-linked genes is partly compensated for by gene-specific up-regulation of X-linked genes. Our results demonstrate that the rate of genetic degeneration of Y-linked genes in S. latifolia is as fast as in animals, and that the evolutionary trajectories of sex chromosomes are similar in the two kingdoms.

LTR retrotransposons in the dioecious plant Silene latifolia

Genome ◽  
2002 ◽  
Vol 45 (4) ◽  
pp. 745-751 ◽  
Author(s):  
Sachihiro Matsunaga ◽  
Fumi Yagisawa ◽  
Maki Yamamoto ◽  
Wakana Uchida ◽  
Shunsuke Nakao ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Evolutionary Dynamics ◽  
Sex Chromosome ◽  
Silene Latifolia ◽  
Ltr Retrotransposons ◽  
Dioecious Plant ◽  
Dioecious Species ◽  
Y Chromosomes ◽  
Genus Silene ◽  
Silene Species

Conserved domains of two types of LTR retrotransposons, Ty1–copia- and Ty3–gypsy-like retrotransposons, were isolated from the dioecious plant Silene latifolia, whose sex is determined by X and Y chromosomes. Southern hybridization analyses using these retrotransposons as probes resulted in identical patterns from male and female genomes. Fluorescence in situ hybridization indicated that these retrotransposons do not accumulate specifically in the sex chromosomes. These results suggest that recombination between the sex chromosomes of S. latifolia has not been severely reduced. Conserved reverse transcriptase regions of Ty1–copia-like retrotransposons were isolated from 13 different Silene species and classified into two major families. Their categorization suggests that parallel divergence of the Ty1–copia-like retrotransposons occurred during the differentiation of Silene species. Most functional retrotransposons from three dioecious species, S. latifolia, S. dioica, and S. diclinis, fell into two clusters. The evolutionary dynamics of retrotransposons implies that, in the genus Silene, dioecious species evolved recently from gynodioecious species.Key words: retrotransposon, dioecious plant, sex chromosome.

Y chromosome specific markers and the evolution of dioecy in the genus Silene

Genome ◽  
1998 ◽  
Vol 41 (2) ◽  
pp. 141-147 ◽  
Author(s):  
Y Hi Zhang ◽  
Veronica S Stilio ◽  
Farah Rehman ◽  
Amy Avery ◽  
David Mulcahy ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Sex Chromosomes ◽  
Silene Latifolia ◽  
Dioecious Species ◽  
Sequence Characterized Amplified Region ◽  
Y Chromosomes ◽  
Heteromorphic Sex Chromosomes ◽  
Males And Females ◽  
Genus Silene ◽  
Evolution Of Dioecy

Sex determination in plants has been most thoroughly investigated in Silene latifolia, a dioecious species possessing heteromorphic sex chromosomes. We have identified several new Y chromosome linked RAPD markers and converted these to more reliable sequence characterized amplified region (SCAR) markers by cloning the RAPD fragments and developing longer primers. Of the primer pairs for seven SCARs, five amplify a single, unique fragment from the DNA of male S. latifolia. Two sets of primers also amplify additional fragments common to males and females. Homology between the X and Y chromosomes is sufficient to allow the amplification of fragments from females under less stringent PCR conditions. Five of the SCARs also distinguish between the sexes of closely related dioecious taxa of the section Elisanthe, but not between the sexes of distantly related dioecious species. These markers will be useful for continued investigations into the evolution of sex, phylogenetic relationships among taxa, and population dynamics of sex ratios in the genus Silene.Key words: Melandrium, RAPDs, sex chromosomes, SCARs.

scholarly journals A selective sweep in or near the Silene latifolia X-linked gene SlssX

2008 ◽  
Vol 90 (1) ◽  
pp. 85-95 ◽  
Author(s):  
D. A. FILATOV
Keyword(s):  
High Frequency ◽  
Selective Sweep ◽  
Selective Advantage ◽  
Silene Latifolia ◽  
Gene Encoding ◽  
Linked Gene ◽  
Compensatory Evolution ◽  
Y Chromosomes ◽  
Strong Homology ◽  
Recent Origin

SummaryThe most prominent feature of Y chromosomes is that they do not recombine and are usually genetically degenerate, containing only a few genes. White campion Silene latifolia has evolved sex chromosomes relatively recently, probably within the last 10–15 million years. Perhaps due to its recent origin, the Y chromosome in this species has not completely degenerated and most isolated X-linked genes have intact Y-linked homologues. A gene encoding a protein with strong homology to spermidine synthases, Slss, is the exception to this rule, as the Y-linked copy of this gene has apparently lost its function. Here I report evidence for a recent selective sweep in the X-linked copy of this gene (SlssX) that could reflect compensatory evolution in an X-linked gene that has lost a functional Y-linked homologue. The spread and fixation of an advantageous mutation in SlssX has resulted in a dramatic loss of genetic diversity and an excess of high-frequency derived polymorphisms in this gene. As the sweep has not affected the closely linked DD44X gene, the selective advantage of the mutation that has driven the sweep in the SlssX gene might have been less than 1%.

C-banded karyotypes of two Silene species with heteromorphic sex chromosomes

Genome ◽  
2002 ◽  
Vol 45 (2) ◽  
pp. 243-252 ◽  
Author(s):  
Aleksandra Grabowska-Joachimiak ◽  
Andrzej Joachimiak
Keyword(s):  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Silene Latifolia ◽  
Silene Dioica ◽  
Dna Amount ◽  
Metaphase Chromosomes ◽  
X Chromosomes ◽  
C Banding ◽  
Y Chromosomes ◽  
Heteromorphic Sex Chromosomes

Mitotic metaphase chromosomes of Silene latifolia (white campion) and Silene dioica (red campion) were studied and no substantial differences between the conventional karyotypes of these two species were detected. The classification of chromosomes into three distinct groups proposed for S. latifolia by Ciupercescu and colleagues was considered and discussed. Additionally, a new small satellite on the shorter arm of homobrachial chromosome 5 was found. Giemsa C-banded chromosomes of the two analysed species show many fixed and polymorphic heterochromatic bands, mainly distally and centromerically located. Our C-banding studies provided an opportunity to better characterize the sex chromosomes and some autosome types, and to detect differences between the two Silene karyotypes. It was shown that S. latifolia possesses a larger amount of polymorphic heterochromatin, especially of the centromeric type. The two Silene sex chromosomes are easily distinguishable not only by length or DNA amount differences but also by their Giemsa C-banding patterns. All Y chromosomes invariably show only one distally located band, and no other fixed or polymorphic bands on this chromosome were observed in either species. The X chromosomes possess two terminally located fixed bands, and some S. latifolia X chromosomes also have an extra-centric segment of variable length. The heterochromatin amount and distribution revealed by our Giemsa C-banding studies provide a clue to the problem of sex chromosome and karyotype evolution in these two closely related dioecious Silene species.Key words: dioecious plant, Silene dioica, Silene latifolia, karyotype, sex chromosomes, heterochromatin, C-banding.

scholarly journals Evolutionary trajectories of three independent neo-sex chromosomes inDrosophila

2021 ◽  
Author(s):  
Masafumi Nozawa ◽  
Yohei Minakuchi ◽  
Kazuhiro Satomura ◽  
Shu Kondo ◽  
Atsushi Toyoda ◽  
...  
Keyword(s):  
X Chromosome ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Gene Loss ◽  
Comparative Genomic ◽  
Functional Constraints ◽  
Evolutionary Trajectory ◽  
Y Chromosomes ◽  
Dead End ◽  
Evolutionary Trajectories

ABSTRACTDosage compensation (DC) on the X chromosome is a mechanism to counteract the deleterious effects by gene loss from the Y chromosome. However, DC cannot work efficiently if the X chromosome also degenerates. This indeed occurs in the neo-sex chromosomes inDrosophila miranda, where neo-X as well as neo-Y chromosomes are under accelerated pseudogenization. To examine the generality of this pattern, we investigated the evolution of two additional neo-sex chromosomes that independently emerged inD. albomicansandD. americanaand compared their evolutionary processes with that inD. miranda. Comparative genomic and transcriptomic analyses revealed that the pseudogenization rate on neo-X is also accelerated in the two species (though lesser extent inD. americana). We also found that neo-X-linked genes whose neo-Y homologs are pseudogenized tend to be upregulated more stringently than those whose neo-Y homologs remain functional. Moreover, the genes under strong functional constraints and highly expressed in the testis tended to remain functional on neo-X and neo-Y, respectively. Focusing on theD. mirandaandD. albomicansneo-sex chromosomes that independently emerged from the same autosome, we further found that the same genes tend to have been pseudogenized in parallel on neo-Y. Those genes includeIdgf6andJhI-26whose functions seem to be unnecessary or could be even harmful for males. These results indicate that neo-sex chromosomes inDrosophilashare a common evolutionary trajectory after their emergence, which may be applicable to other sex chromosomes in a variety of organisms to avoid being an evolutionary dead-end.

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