Drosophila X-Linked Genes Have Lower Translation Rates than Autosomal Genes.
In Drosophila, X-linked and autosomal genes achieve comparable expression at the mRNA level. Whether comparable X-autosome gene expression is realized at the translational and, ultimately, the protein levels is, however, unknown. Previous studies suggest the possibility of higher translation rates for X-linked genes owing to stronger usage of preferred codons. In this study, we use public ribosome profiling data from Drosophila melanogaster to infer translation rates on the X chromosome versus the autosomes. We find that X-linked genes have consistently lower ribosome densities than autosomal genes in S2 cells, early embryos, eggs, and mature oocytes. Surprisingly, the lower ribosome densities of X-linked genes are not consistent with faster translation elongation but instead imply slower translation initiation. In particular, X-linked genes have sequence features known to slow translation initiation such as stronger mRNA structure near start codons and longer 5'-UTRs. Comparison to outgroup species suggests that stronger mRNA structure is an evolved feature of Drosophila X chromosomes. Finally, we find that the magnitude of the X-autosome difference in ribosome densities is smaller for genes encoding members of protein complexes, suggesting that stoichiometry constrains the evolution of translation rates. In sum, our analyses suggest that Drosophila X-linked genes have evolved lower translation rates than autosomal genes despite stronger usage of preferred codons.
Department of Biology, University of Rochester zhangz.sci@gmail.com.
Zhenguo
Z
Zhang
Department of Biology, University of Rochester.
Daven C
DC
Presgraves
D000818:Animals; D059006:Chromosomes, Insect; D003062:Codon; D004330:Drosophila / Q000235:genetics* / Q000378:metabolism; D019143:Evolution, Molecular; D017344:Genes, Insect; D050172:Genes, X-Linked; D009690:Nucleic Acid Conformation; D014176:Protein Biosynthesis; D012333:RNA, Messenger / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D012270:Ribosomes / Q000378:metabolism; D014960:X Chromosome
D003062:Codon; D012333:RNA, Messenger
Drosophila; codon usage bias; sex chromosome; translation rates