Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression

Abstract

Descriptions of recently evolved genes suggest several mechanisms of origin including exon shuffling, gene fission/fusion, retrotransposition, duplication-divergence, and lateral gene transfer, all of which involve recruitment of preexisting genes or genetic elements into new function. The importance of noncoding DNA in the origin of novel genes remains an open question. We used the well annotated genome of the genetic model system Drosophila melanogaster and genome sequences of related species to carry out a whole-genome search for new D. melanogaster genes that are derived from noncoding DNA. Here, we describe five such genes, four of which are X-linked. Our RT-PCR experiments show that all five putative novel genes are expressed predominantly in testes. These data support the idea that these novel genes are derived from ancestral noncoding sequence and that new, favored genes are likely to invade populations under selective pressures relating to male reproduction.

Fig. 1.

Southern blot analysis of putative novel genes in D. melanogaster (mel), D. simulans (sim), D. yakuba (yak), D. erecta (ere), and D. ananassae (ana). D, Dde; H, HhaI. Asterisks indicate predicted band sizes of focal genes. There are no predicted band sizes for CG32582 in D. simulans because of a gap in the assembly.

Fig. 2.

List of novel genes, chromosome number, coordinates, amino acid number, and gene models. Black boxes indicate coding regions. Gray boxes indicate untranslated regions.

Fig. 3.

RT-PCR analysis of five putative novel genes in D. melanogaster. T, testes; RTR, reproductive tract remainder (male reproductive tract minus testes); C, male carcass (adult male minus reproductive tract); WF, whole female.

Fig. 4.

Paralogous regions associated with novel genes. Parallel solid lines indicate homology among flanking regions of focal genes. Filled rectangular box indicates gene region. Distances between focal gene and paralogous copy are indicated. CG15323 seems to be part of a larger, noncoding “family” of copies (only most closely related sequence is shown). CG32712 returned no significant nonself blast hits. Homologous sequence for all other genes as well as the paralogous copies was found in D. simulans, suggesting that most duplications occurred along the lineage leading to D. melanogaster and D. simulans. D. simulans contains a region homologous to the D. melanogaster gene CG32690 but has no homologous ORF. This D. simulans sequence, using blat, points to chromosome X_random, making unclear the distance between two D. simulans copies. Extensive indel variation among paralogous copies of the CG32690 gene and CG32582 region disallowed calculation of percentage identity. D. simulans sequence homologous to the CG32582 gene region occurs in a currently unassembled region in D. simulans genome.