Meiotic Sex Chromosome Inactivation: Compensation by Gene Traffic

Long, Manyuan; Emerson, J. J.

doi:10.1016/j.cub.2017.05.077

Cited by 9 publications

(7 citation statements)

References 19 publications

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“…This pattern was confirmed for various organisms such as flies (Betrán et al, 2002;Dai et al, 2006;Bai et al, 2007;Zhang et al, 2010), mosquitos (Toups and Hahn, 2010), and mammals (Emerson et al, 2004;Carelli et al, 2016). The preferential fixation of male-biased duplicated copies into autosomes likely reflects the fact that, during spermatogenesis, the silencing of X chromosome in meiosis and later stages, as observed in mammals (Richler et al 1992) and Drosophila (Vibranovski et al, 2009b;Mahadevaraju et al, 2021) provided a selective mechanism to drive the X to A gene traffic in new gene duplication (Vibranovski et al, 2009a;Jiang et al, 2017;Long and Emerson et al, 2017). Consequently, natural selection favors the fixation of autosomal duplicate copies that escape the X chromosome and compensate for the expression of its parental gene (Betrán et al, 2002;Vibranovski et al, 2009aVibranovski et al, , 2012Casola and Betrán, 2017).…”

Section: Introductionmentioning

confidence: 77%

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Rapid gene evolution in an ancient post-transcriptional and translational regulatory system compensates for meiotic X chromosomal inactivation

Xia

Ventura

Blaha

et al. 2021

Preprint

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It is conventionally assumed that conserved pathways evolve slowly with little participation of gene evolution. Nevertheless, it has been recently observed that young genes can take over fundamental functions in essential biological processes, for example, development and reproduction. It is unclear how newly duplicated genes are integrated into ancestral networks and reshape the conserved pathways of important functions. Here, we investigated origination and function of two autosomal genes that evolved recently in Drosophila: Poseidon and Zeus, which were created by RNA-based duplications from the X-linked CAF40, a subunit of the conserved CCR4-NOT deadenylase complex involved in post-transcriptional and translational regulation. Knockdown and knockout assays show that the two genes quickly evolved critically important functions in viability and male fertility. Moreover, our transcriptome analysis demonstrates that the three genes have a broad and distinct effect in the expression of hundreds of genes, with almost half of the differentially expressed genes being perturbed exclusively by one paralog, but not the others. Co-immunoprecipitation and tethering assays show that the CAF40 paralog Poseidon maintains the ability to interact with the CCR4-NOT deadenylase complex and might act in post-transcriptional mRNA regulation. The rapid gene evolution in the ancient post-transcriptional and translational regulatory system may be driven by evolution of sex chromosomes to compensate for the meiotic X chromosomal inactivation (MXCI) in Drosophila.

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Section: Introductionmentioning

confidence: 77%

“…Poseidon may compensate for CAF40 whose expression is suppressed by MXCI, similar to the function of the autosomal retroposed RPL10L in humans (Jiang et al, 2017. Long andEmerson, 2017). However, Zeus is not completely redundant to Poseidon.…”

Section: Discussionmentioning

confidence: 94%

Rapid gene evolution in an ancient post-transcriptional and translational regulatory system compensates for meiotic X chromosomal inactivation

Xia

Ventura

Blaha

et al. 2021

Preprint

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“…Given the divergence of Zeus from Poseidon , these data suggest likely different roles of the two paralogs. Poseidon may compensate for CAF40 whose expression is suppressed by MXCI, similar to the function of the autosomal retroposed RPL10L in humans ( Jiang et al 2017 ; Long and Emerson 2017 ). However, Zeus is not completely redundant to Poseidon .…”

Section: Discussionmentioning

confidence: 89%

“…This pattern was confirmed for various organisms such as flies ( Betran et al 2002 ; Dai et al 2006 ; Bai et al 2007 ; Zhang et al 2010 ), mosquitos ( Toups and Hahn 2010 ), and mammals ( Emerson et al 2004 ; Carelli et al 2016 ). The preferential fixation of male-biased duplicated copies into autosomes likely reflects the fact that, during spermatogenesis, the silencing of X chromosome in meiosis and later stages, as observed in mammals ( Richler et al 1992 ) and Drosophila ( Vibranovski, Zhang, et al 2009 ; Mahadevaraju et al 2021 ) provided a selective mechanism to drive the X to A gene traffic in new gene duplication ( Vibranovski, Lopes, et al 2009 ; Jiang et al 2017 ; Long and Emerson 2017 ). Consequently, natural selection favors the fixation of autosomal duplicate copies that escape the X chromosome and compensate for the expression of its parental gene ( Betran et al 2002 ; Vibranovski, Lopes, et al 2009 , 2012; Casola and Betran 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Rapid Gene Evolution in an Ancient Post-transcriptional and Translational Regulatory System Compensates for Meiotic X Chromosomal Inactivation

Xia

Ventura

Blaha

et al. 2021

Molecular Biology and Evolution

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Summary It is conventionally assumed that conserved pathways evolve slowly with little participation of gene evolution. Nevertheless, it has been recently observed that young genes can take over fundamental functions in essential biological processes, for example, development and reproduction. It is unclear how newly duplicated genes are integrated into ancestral networks and reshape the conserved pathways of important functions. Here, we investigated origination and function of two autosomal genes that evolved recently in Drosophila: Poseidon and Zeus, which were created by RNA-based duplications from the X-linked CAF40, a subunit of the conserved CCR4-NOT deadenylase complex involved in post-transcriptional and translational regulation. Knockdown and knockout assays show that the two genes quickly evolved critically important functions in viability and male fertility. Moreover, our transcriptome analysis demonstrates that the three genes have a broad and distinct effect in the expression of hundreds of genes, with almost half of the differentially expressed genes being perturbed exclusively by one paralog, but not the others. Co-immunoprecipitation and tethering assays show that the CAF40 paralog Poseidon maintains the ability to interact with the CCR4-NOT deadenylase complex and might act in post-transcriptional mRNA regulation. The rapid gene evolution in the ancient post-transcriptional and translational regulatory system may be driven by evolution of sex chromosomes to compensate for the meiotic X chromosomal inactivation (MXCI) in Drosophila.

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“…Second, duplication permits sex-biased partitioning to precede the shift of a trait fitness value. For example, retrogenes successfully escaping the X chromosome in mammals immediately cease existing in an environment subject to meiotic X-inactivation, a process specific to male biology (Long and Emerson 2017). In the evolution of UV color vision, the path to the phenotype shift and the sex-specificity did not happen simultaneously so the pleiotropy model is a poor fit.…”

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confidence: 99%

Sex-linked gene traffic underlies the acquisition of sexually dimorphic UV color vision in Heliconius butterflies

Chakraborty

Lara

Dang

et al. 2022

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Butterflies have photoreceptor cells that are sensitive to the ultraviolet part of the spectrum due to ultraviolet-sensitive rhodopsin (UVRh), a gene that has been duplicated in the Heliconius genus. In individuals expressing UVRh1 and UVRh2, electrophysiological and behavioral studies demonstrate that these opsin proteins enable discrimination of UV wavelengths. This behavioral trait varies between species, being absent in H. melpomene and limited to females in H. erato. To identify the evolutionary origins of this trait, we first examined UV color vision in H. charithonia, a species related to H. erato in the sara/sapho group. We found that this species also has sexually dimorphic UV color vision. To identify the genetic basis of this trait, we built a reference-grade genome assembly of H. charithonia. We discovered that one duplicate, UVRh1, is present on the W chromosome, making it obligately female-specific. We employed gDNA PCR assays of UVRh1 across the Heliconius genus. In species with sexually dimorphic UVRh1 mRNA expression, UVRh1 gDNA is absent in males, whereas in species with sexually monomorphic UVRh1 mRNA expression, UVRh1 gDNA is found in both sexes. The presence or absence of male UVRh1 expression across the Heliconius phylogeny supports a model where sexual dimorphism was acquired early via movement of a gene duplication to the W-chromosome. We used CRISPR-Cas9 to engineer a deletion in the UVRh1 locus in female H. charithonia and use immunohistochemistry to show that UVRh1 protein expression is absent in mutant tissue, similar to that of males. Our results show that a rare behavioral phenotype, sex-specific UV color vision, was acquired via sex chromosome gene traffic of a duplicated UV rhodopsin.

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Meiotic Sex Chromosome Inactivation: Compensation by Gene Traffic

Cited by 9 publications

References 19 publications

Rapid gene evolution in an ancient post-transcriptional and translational regulatory system compensates for meiotic X chromosomal inactivation

Rapid gene evolution in an ancient post-transcriptional and translational regulatory system compensates for meiotic X chromosomal inactivation

Rapid Gene Evolution in an Ancient Post-transcriptional and Translational Regulatory System Compensates for Meiotic X Chromosomal Inactivation

Sex-linked gene traffic underlies the acquisition of sexually dimorphic UV color vision in Heliconius butterflies

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