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Drcd-1 related: a positively selected spermatogenesis retrogene in Drosophila

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Abstract

Gene duplication is a major force driving genome evolution, and examples of this mode of evolution and of the functions of duplicated genes are needed to reveal general patterns. Here, our study focuses on a particular retrogene (i.e., CG9573) that originated about 5–13 million years ago that we have named Drcd-1 related. It originated in Drosophila through retroposition of the parental gene Required for cell differentiation 1 of Drosophila (Drcd-1; CG14213), which is a known transcription cofactor. Drcd-1r is only present in D. melanogaster, D. simulans, D. sechellia, and D. mauritiana. Drcd-1r is an X to autosome retroposition event. Many retrogenes are X to autosome copies and it has been shown that positive selection underlies this bias. We sought to understand Drcd-1r mode of evolution and function to contribute to the understanding of the selective pressures acting on X to autosome retrogenes. Drcd-1r overlaps with another gene, it is within the 3′ UTR of the gene CG13102 and is encoded in the opposite orientation. We have studied the characteristics of the transcripts and quantified expression of CG13102 and Drcd-1r in wild-type flies. We found that Drcd-1r is transcribed specifically in testes. We also studied the molecular evolution of Drcd-1r and Drcd-1 and found that the parental gene has evolved under very strong purifying selection but the retrogene has evolved very rapidly (Ka/Ks ~1) under both positive and purifying selection, as revealed using divergence and polymorphism data. These results indicate that Drcd-1r has a novel function in the Drosophila testes. To further explore Drcd-1r function we used a strain containing a P element inserted in the region where CG13102 and Drcd-1r are located that shows recessive male sterility. Analysis of this strain reveals the difficulties that can be encountered in studying the functions of genes with overlapping transcripts. Avenues for studying of the function of this gene are proposed.

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Acknowledgments

We thank Dr. Chitra Chandrasekaran, Sidi Chen and Dr. Manyuan Long for comments on this work. We also thank Mao-Lien Wu, Chung-I Wu, Tessa Bauer DuMont and Chip Aquadro for providing stocks. Research was supported by UTA startup funds and grant R01 GM071813 from the National Institutes of Health, USA to EB.

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  1. Department of Biology, University of Texas at Arlington, Box 19498, Arlington, TX, 76019, USA

    Jorge Ernesto Quezada-Díaz, Taniya Muliyil, Javier Río & Esther Betrán

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  1. Jorge Ernesto Quezada-Díaz
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Correspondence to Esther Betrán.

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10709_2010_9474_MOESM1_ESM.pdf

Supplementary Figure 1. Alignment of genomic regions of Drcd-1 and Drcd-1r. The alignment shows ATG and stop codons for both genes. Note that sequence conservation exists only in the CDS. Sequence conservation does not extend to other gene regions (i.e., UTRs). Neither remnants of poly-A tract nor direct repeats remain in the retrogene insertion site. The non-homologous 3’ region is shown in blue. (PDF 23 kb)

10709_2010_9474_MOESM2_ESM.pdf

Supplementary Figure 2. Drcd-1r genomic region. The genomic organization of the region where Drcd-1r is inserted is given as annotated in FlyBase. CDS regions are in bold. The Drcd-1r (CG9573) sequence has been reversed and complemented. The location of the P element insertion of line 11773 is also shown. (PDF 39 kb)

10709_2010_9474_MOESM3_ESM.pdf

Supplementary Figure 3. Drcd-1r alignment between species. Potentially positively selected codons are highlighted in blue. (PDF 27 kb)

10709_2010_9474_MOESM4_ESM.pdf

Supplementary Figure 4. Alignment of D. melanogaster Drcd-1r and Drcd-1 with human Rcd-1. Amino acids that participate in dimerization in humans are highlighted in green. Amino acids of the positively charged cleft that binds DNA in humans are highlighted in blue. Residues are highlighted in Drosophila genes in either green or blue if conserved. Differences between Rcd-1 and Drcd-1r proteins are highlighted in red. (PDF 30 kb)

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Quezada-Díaz, J.E., Muliyil, T., Río, J. et al. Drcd-1 related: a positively selected spermatogenesis retrogene in Drosophila. Genetica 138, 925–937 (2010). https://doi.org/10.1007/s10709-010-9474-8

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