The origin of the Jingwei gene and the complex modular structure of its parental gene, yellow emperor, in Drosophila melanogaster

Jingwei (igM) is the first gene found to be of sufficiently recent origin i n Drosophila to offer insights into the origin of a gene. While its chimeri cal gene structure was partially resolved as including a retrosequence of a lcohol dehydrogenase (Adh), the structure of its non-Adh parental gene, the donor of the N-terminal domain of jgw: is unclear. We characterized this n on-Adh parental locus, yellow emperor (ymp), by cloning it, mapping it onto the polytene chromosomes, sequencing the entire locus, and examining its e xpression patterns in Drosophila melanogaster. We show that ymp is located in the 96-E region; the N-terminal domain of ymp, has donated the non-Adh p ortion of jgw via a duplication. The similar 5' portions of the gene and it s regulatory sequences give rise to similar testis-specific expression patt erns in ymp and jgw in Drosophila teissieri. Furthermore, between-species c omparison of ymp, revealed purifying selection in the protein sequence, sug gesting a functional constraint in ymp. While the structure of ymp provides clear information for the molecular origin of the new gene jgw, it unexpec tedly casts a new light on the concept of genes. We found, for the first ti me, that the single locus of the ymp gene encompasses three major molecular mechanisms determining structure of eukaryotic genes: (1) the 5' exons of pmp are involved in an exon-shuffling event that has created the portion re cruited by jgw; (2) using alternative cleavage sites and alternative splici ng sites, the 3' exon groups of ymp produce two proteins with nonhomologous C-terminal domains, both exclusively in the testis; and (3) in the opposit e strand of the third intron of ymp is an essential gene, musashi (msi), wh ich encodes an RNA-binding protein. The composite gene structure of ymp man ifests the complexity of the gene concept, which should be considered in ge nomic research, e.g., gene finding.