On the possible role of tRNA base modifications in the evolution of codon usage: queuosine and Drosophila

Abstract

The best documented selection-based hypothesis to explain unequal usage of codons is based on the relative abundance of isoaccepting tRNAs. In unicellular organisms the most used codons are optimally translated by the most abundant tRNAs. The chemical bonding energies are affected by modification of the four traditional bases, in particular in the first anti-codon corresponding to the third codon position. One nearly universal modification is queuosine (Q) for guanine (G) in tRNA(His), tRNA(Asp), tRNA(Asn), and tRNA(Tyr); this changes the optimal binding from codons ending in C to no preference or a slight preference for U-ending codons. Among species of Drosophila, codon usage is constant with the exception of the Drosophila willistoni lineage which has shifted primary usage from C-ending codons to U/T ending codons only for these four amino acids. In Drosophila melanogaster Q containing tRNAs only predominate in old adults. We asked the question whether in D. willistoni these Q containing tRNAs might predominate earlier in development. As a surrogate for levels of modification we studied the expression of the gene (tgt) coding for the enzyme that catalyzes the substitution of Q for G in different life stages of D. melanogaster, D. pseudoobscura, and D. willistoni. Unlike the other two species, the highest tgt expression in D. willistoni is in young females producing eggs. Because tRNAs laid down in eggs persist through the early stages of development, this implies that Q modification occurs earlier in development in D. willistoni than in other Drosophila.