A long-term demasculinization of X-linked intergenic noncoding RNAs in Drosophila melanogaster

Gao, Ge; Vibranovski, Maria D.; Zhang, Li; Li, Zheng; Liu, Min; Zhang, Yong E.; Li, Xinmin; Zhang, Wenxia; Fan, Qing; VanKuren, Nicholas W.; Long, Manyuan; Wei, Liping

doi:10.1101/gr.165837.113

Cited by 24 publications

(31 citation statements)

References 53 publications

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“…As an interesting contrast to our finding of Y-linked genes with male-limited expression, Baker et al [42] found genes only expressed in males to be enriched on the X chromosome of stalk-eyed flies. Their result seems more surprising than ours, and runs counter to the feminization (or demasculization) of expression patterns of X-linked genes reported in other studies [43][44][45]. Nevertheless, it is unclear how often we ought to expect genes with male-limited expression to be on the Y chromosome.…”

Section: Identification Of Y-linked Markerscontrasting

confidence: 99%

The Size and Content of the Sex-Determining Region of the Y Chromosome in Dioecious Mercurialis annua, a Plant with Homomorphic Sex Chromosomes

Veltsos¹,

Cossard²,

Beaudoing³

et al. 2018

Preprint

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Many dioecious plants have sex chromosomes that are cytologically heteromorphic, but about half of species lack cytological differences between males and females and are thus homomorphic. Very little is known about the size and content of the non-recombining sex-determining region (SDR) in these species. Here, we assess the size and content of the SDR of the diploid dioecious herb Mercurialis annua, which has homomorphic sex chromosomes and shows signatures of mild Y-chromosome degeneration. We used RNAseq to identify new Y-linked markers for M. annua. Twelve of 24 transcripts with male-specific and male-biased expression could only be PCR-amplified from males and are thus Y-linked. We found a further six Y-linked sequences that were present in males but not females using genome capture data from multiple populations. We used the Y-linked sequences to identify and sequence 17 sex-linked bacterial artificial chromosomes (BACs), which form 11 groups of non-overlapping sequence, covering a total sequence length of about 1.5 Mb. Content analysis of this region suggests it is enriched for repeats, has a low gene density and contains few candidate sex-determining genes. The BACs map to a subset of the sex-linked region of the genetic map, which is estimated to be at least 14.5 Mb. This is substantially larger than estimates for other dioecious plants with homomorphic sex chromosomes, especially given the small genome size of M. annua. Our data provide a rare, high-resolution view of the homomorphic Y chromosome of a dioecious plant.

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Section: Identification Of Y-linked Markerscontrasting

confidence: 99%

The Size and Content of the Sex-Determining Region of the Y Chromosome in Dioecious Mercurialis annua, a Plant with Homomorphic Sex Chromosomes

Veltsos¹,

Cossard²,

Beaudoing³

et al. 2018

Preprint

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“…Older male-biased genes are underrepresented on the Drosophila X chromosome, while younger male-biased genes [those emerged after the melanogaster split 3-6 million years ago (Russo et al 1995)] are enriched (Zhang et al 2010). This suggests that X demasculinization is an evolutionary process (Gao et al 2014). While enrichment of female-biased genes on the X is predicted, demasculinization of the X opposes the expectation that malebenefitting genes should accumulate on the X chromosome (Rice 1984).…”

mentioning

confidence: 50%

Sex-Biased Gene Expression and Evolution of the X Chromosome in Nematodes

et al. 2014

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Studies of X chromosome evolution in various organisms have indicated that sex-biased genes are nonrandomly distributed between the X and autosomes. Here, to extend these studies to nematodes, we annotated and analyzed X chromosome gene content in four Caenorhabditis species and in Pristionchus pacificus. Our gene expression analyses comparing young adult male and female mRNAseq data indicate that, in general, nematode X chromosomes are enriched for genes with high female-biased expression and depleted of genes with high male-biased expression. Genes with low sex-biased expression do not show the same trend of X chromosome enrichment and depletion. Combined with the observation that highly sex-biased genes are primarily expressed in the gonad, differential distribution of sex-biased genes reflects differences in evolutionary pressures linked to tissue-specific regulation of X chromosome transcription. Our data also indicate that X dosage imbalance between males (XO) and females (XX) is influential in shaping both expression and gene content of the X chromosome. Predicted upregulation of the single male X to match autosomal transcription (Ohno's hypothesis) is supported by our observation that overall transcript levels from the X and autosomes are similar for highly expressed genes. However, comparison of differentially located one-to-one orthologs between C. elegans and P. pacificus indicates lower expression of X-linked orthologs, arguing against X upregulation. These contradicting observations may be reconciled if X upregulation is not a global mechanism but instead acts locally on a subset of tissues and X-linked genes that are dosage sensitive. IN an XY sex-determination system, male and female genomes are identical with the exception of the male-specific Y chromosome, which bears few genes (Charlesworth et al. 2005). This is particularly true when the Y chromosome is thought to be completely lost, as is the case for C. elegans and many other nematodes (Walton 1940). Because gene content is the same, phenotypic differences between males and females, termed "sexual dimorphisms," must be caused by differential gene expression between the two sexes (Connallon and Knowles 2005;Ellegren and Parsch 2007). Throughout the article, such differentially expressed genes are referred to as "sex biased." As males and females have different fitness optima, a trait that is beneficial to one sex can be harmful to the other (termed sexual antagonism) (Rice and Chippindale 2001;Arnqvist 2004;Connallon and Knowles 2005;Ellegren and Parsch 2007;Mank et al. 2008a;Rice 1984). The evolution of sex-biased gene expression is thought to mediate the effects of sexual antagonism and allow for achievement of sex-specific fitness. Previous studies have indicated that anywhere between 30 and 60% of metazoan genes may be sex biased Parisi et al. 2004;Reinke et al. 2004;Yang et al. 2006;Reinius et al. 2008;Small et al. 2009;Innocenti and Morrow 2010;Assis et al. 2012;Reinius et al. 2012;Thomas et al. 2012). Genes with sex-biased exp...

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“…A study in Drosophila revealed that a large proportion of intergenic regions encode ncRNAs and that particularly early stages of development express most abundant species of ncRNAs [86] . A recent study showed that in Drosophila many of these long ncRNAs are male-biased and preferentially associate with autosomes [87] . In the lepidopteran species Bombyx mori , a W-linked long non-coding RNA has been even implicated in acting as the primary signal in sex determination [57] .…”

Section: Resultsmentioning

confidence: 99%

De Novo Assembly and Transcriptome Analysis of the Mediterranean Fruit Fly Ceratitis capitata Early Embryos

et al. 2014

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The agricultural pest Ceratitis capitata, also known as the Mediterranean fruit fly or Medfly, belongs to the Tephritidae family, which includes a large number of other damaging pest species. The Medfly has been the first non-drosophilid fly species which has been genetically transformed paving the way for designing genetic-based pest control strategies. Furthermore, it is an experimentally tractable model, in which transient and transgene-mediated RNAi have been successfully used. We applied Illumina sequencing to total RNA preparations of 8–10 hours old embryos of C. capitata, This developmental window corresponds to the blastoderm cellularization stage. In summary, we assembled 42,614 transcripts which cluster in 26,319 unique transcripts of which 11,045 correspond to protein coding genes; we identified several hundreds of long ncRNAs; we found an enrichment of transcripts encoding RNA binding proteins among the highly expressed transcripts, such as CcTRA-2, known to be necessary to establish and, most likely, to maintain female sex of C. capitata. Our study is the first de novo assembly performed for Ceratitis capitata based on Illumina NGS technology during embryogenesis and it adds novel data to the previously published C. capitata EST databases. We expect that it will be useful for a variety of applications such as gene cloning and phylogenetic analyses, as well as to advance genetic research and biotechnological applications in the Medfly and other related Tephritidae.

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A long-term demasculinization of X-linked intergenic noncoding RNAs in Drosophila melanogaster

Cited by 24 publications

References 53 publications

The Size and Content of the Sex-Determining Region of the Y Chromosome in Dioecious <em>Mercurialis annua</em>, a Plant with Homomorphic Sex Chromosomes

The Size and Content of the Sex-Determining Region of the Y Chromosome in Dioecious <em>Mercurialis annua</em>, a Plant with Homomorphic Sex Chromosomes

Sex-Biased Gene Expression and Evolution of the X Chromosome in Nematodes

De Novo Assembly and Transcriptome Analysis of the Mediterranean Fruit Fly Ceratitis capitata Early Embryos

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