Non-random genomic integration - an intrinsic property of retrogenes in Drosophila?

Metta, Muralidhar; Schlötterer, Christian

doi:10.1186/1471-2148-10-114

Cited by 14 publications

(61 citation statements)

References 36 publications

(39 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…However, a recent study indicates that retroposing genes with diverse expression biases all show an affinity toward autosomes [15]; therefore the apparent 'exodus' of male-biased genes from the X , previously considered as the major indirect evidence for MSCI in flies [1], is not necessarily driven by sexual selection. Earlier studies did show that not only testis-biased, but also somatic male-biased genes are underrepresented on the X [42], but the possible role of these genes in sexual selection could still be invoked with certain ease owing to their sex bias.…”

Section: Discussionmentioning

confidence: 99%

Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome

2011

View full text Add to dashboard Cite

BackgroundPaucity of male-biased genes on the Drosophila X chromosome is a well-established phenomenon, thought to be specifically linked to the role of these genes in reproduction and/or their expression in the meiotic male germline. In particular, meiotic sex chromosome inactivation (MSCI) has been widely considered a driving force behind depletion of spermatocyte-biased X-linked genes in Drosophila by analogy with mammals, even though the existence of global MCSI in Drosophila has not been proven.ResultsMicroarray-based study and qRT-PCR analyses show that the dynamics of gene expression during testis development are very similar between X-linked and autosomal genes, with both showing transcriptional activation concomitant with meiosis. However, the genes showing at least ten-fold expression bias toward testis are significantly underrepresented on the X chromosome. Intriguingly, the genes with similar expression bias toward tissues other than testis, even those not apparently associated with reproduction, are also strongly underrepresented on the X. Bioinformatics analysis shows that while tissue-specific genes often bind silencing-associated factors in embryonic and cultured cells, this trend is less prominent for the X-linked genes.ConclusionsOur data show that the global meiotic inactivation of the X chromosome does not occur in Drosophila. Paucity of testis-biased genes on the X appears not to be linked to reproduction or germline-specific events, but rather reflects a general underrepresentation of tissue-biased genes on this chromosome. Our analyses suggest that the activation/repression switch mechanisms that probably orchestrate the highly-biased expression of tissue-specific genes are generally not efficient on the X chromosome. This effect, probably caused by dosage compensation counteracting repression of the X-linked genes, may be the cause of the exodus of highly tissue-biased genes to the autosomes.

show abstract

Section: Discussionmentioning

confidence: 99%

Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome

2011

View full text Add to dashboard Cite

show abstract

“…Two main explanations have been given for the excess of retrotransposition involving the X chromosome: escape from meiotic sex chromosome inactivation (Betrán et al 2002;Vibranovski et al 2009a) and sexually antagonistic selection against male-favorable genes (Ranz et al 2003;Wu and Xu 2003;Vicoso and Charlesworth 2006). In addition, nonadaptive explanations-such as biased integration of reverse-transcribed cDNAs onto autosomes (Metta and Schlotterer 2010)-have been put forward, though studies of the movement of pseudogenized retrogenes in both Drosophila and mammals have not found any biased integration (Emerson et al 2004;Potrzebowski et al 2008;Meisel 2009), nor has such a bias been observed with respect to transposable elements (Fontanillas et al 2007). Much of the evidence for selection driving retrogenes off the X has been correlative: Such retrogenes often have testis-biased or even testis-specific gene expression, a pattern consistent with the advantage of autosomal copies that are not precociously silenced during spermatogenesis (Betrán et al 2002;Vibranovski et al 2009a).…”

mentioning

confidence: 99%

Genome-wide analysis of retrogene polymorphisms in Drosophila melanogaster

Schrider¹,

Stevens²,

Cardeno³

et al. 2011

Genome Res.

View full text Add to dashboard Cite

Gene duplication via retrotransposition has been shown to be an important mechanism in evolution, affecting gene dosage and allowing for the acquisition of new gene functions. Although fixed retrotransposed genes have been found in a variety of species, very little effort has been made to identify retrogene polymorphisms. Here, we examine 37 Illuminasequenced North American Drosophila melanogaster inbred lines and present the first ever data set and analysis of polymorphic retrogenes in Drosophila. We show that this type of polymorphism is quite common, with any two gametes in the North American population differing in the presence or absence of six retrogenes, accounting for~13% of gene copynumber heterozygosity. These retrogenes were identified by a straightforward method that can be applied using any type of DNA sequencing data. We also use a variant of this method to conduct a genome-wide scan for intron presence/absence polymorphisms, and show that any two chromosomes in the population likely differ in the presence of multiple introns. We show that these polymorphisms are all in fact deletions rather than intron gain events present in the reference genome.

show abstract

“…The recent study by Metta and Schlötterer [21] proposed a new interpretation which negated the need for selection-based hypotheses to understand the out-of-the X movement pattern of Drosophila retrogenes. To test the general role of natural selection, Metta and Schlötterer [21] identified retrogenes for which the parental gene has been lost or degenerated.…”

Section: Introductionmentioning

confidence: 99%

“…To test the general role of natural selection, Metta and Schlötterer [21] identified retrogenes for which the parental gene has been lost or degenerated. In other words, the parental genes and retrogenes are never found in the same species.…”

Section: Introductionmentioning

confidence: 99%

Segmental dataset and whole body expression data do not support the hypothesis that non-random movement is an intrinsic property of Drosophila retrogenes

et al. 2012

View full text Add to dashboard Cite

BackgroundSeveral studies in Drosophila have shown excessive movement of retrogenes from the X chromosome to autosomes, and that these genes are frequently expressed in the testis. This phenomenon has led to several hypotheses invoking natural selection as the process driving male-biased genes to the autosomes. Metta and Schlötterer (BMC Evol Biol 2010, 10:114) analyzed a set of retrogenes where the parental gene has been subsequently lost. They assumed that this class of retrogenes replaced the ancestral functions of the parental gene, and reported that these retrogenes, although mostly originating from movement out of the X chromosome, showed female-biased or unbiased expression. These observations led the authors to suggest that selective forces (such as meiotic sex chromosome inactivation and sexual antagonism) were not responsible for the observed pattern of retrogene movement out of the X chromosome.ResultsWe reanalyzed the dataset published by Metta and Schlötterer and found several issues that led us to a different conclusion. In particular, Metta and Schlötterer used a dataset combined with expression data in which significant sex-biased expression is not detectable. First, the authors used a segmental dataset where the genes selected for analysis were less testis-biased in expression than those that were excluded from the study. Second, sex-biased expression was defined by comparing male and female whole-body data and not the expression of these genes in gonadal tissues. This approach significantly reduces the probability of detecting sex-biased expressed genes, which explains why the vast majority of the genes analyzed (parental and retrogenes) were equally expressed in both males and females. Third, the female-biased expression observed by Metta and Schlötterer is mostly found for parental genes located on the X chromosome, which is known to be enriched with genes with female-biased expression. Fourth, using additional gonad expression data, we found that autosomal genes analyzed by Metta and Schlötterer are less up regulated in ovaries and have higher chance to be expressed in meiotic cells of spermatogenesis when compared to X-linked genes.ConclusionsThe criteria used to select retrogenes and the sex-biased expression data based on whole adult flies generated a segmental dataset of female-biased and unbiased expressed genes that was unable to detect the higher propensity of autosomal retrogenes to be expressed in males. Thus, there is no support for the authors’ view that the movement of new retrogenes, which originated from X-linked parental genes, was not driven by selection. Therefore, selection-based genetic models remain the most parsimonious explanations for the observed chromosomal distribution of retrogenes.

show abstract

Non-random genomic integration - an intrinsic property of retrogenes in Drosophila?

Cited by 14 publications

References 36 publications

Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome

Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome

Genome-wide analysis of retrogene polymorphisms in Drosophila melanogaster

Segmental dataset and whole body expression data do not support the hypothesis that non-random movement is an intrinsic property of Drosophila retrogenes

Contact Info

Product

Resources

About