Apis Melifera

Copyright 0 1993 by the Genetics Society of America

The Mitochondrial Genome of the Honeybee Apis melliferu: Complete Sequence and Genome Organization
R. H. Crozier and Y. C. Crozier
Department o Genetics and Human Variation, La Trobe University, Bundoora, Victoria 3083, Australia f Manuscript received June 12, 1992 Accepted for publication October 3, 1992

ABSTRACT The complete sequenceof honeybee (Apis mellqera)mitochondrial DNA is reported being 16,343 bp long in the strain sequenced. Relative to their positions in the Drosophila map, 1 1 of the tRNA genes are in altered positions, but the other genes and regions are in the same relative positions. Comparisons of the predicted protein sequences indicate that the honeybee mitochondrial genetic code is the same as that forDrosophila; but the anticodons of two tRNAs differ between these two insects. The base composition shows extreme bias, being 84.9% AT(cf. 78.6% in Drosophila yakuba). In protein-encoding genes, the AT bias is strongest at the thirdcodon positions (which in some cases lack guanines altogether), and least in second codon positions. Multiple stepwise regression analysis of the predicted products of theprotein-encoding genes shows a significant association between the numbers of occurrences of amino acids and %Tin codon family, but not with the number of codons per codon family or other parameters associated with codon family base composition. Differences in amino acid abundances are apparent between the predicted Apis and Drosophila proteins, with a relative abundance in the Apis proteins oflysine and a relative deficiency of alanine. Drosophila alanine residues are as often replaced by serine as conserved in Apis. The differences in abundances between Drosophila and Apis are associated with %AT in the codon families, and the degree of divergence in amino acid composition between proteins correlates with the divergence in %AT at the second codon positions. Overall, transversions areabouttwice as abundant as transitions when comparing Drosophila and Apis protein-encoding genes,but this ratio varies between codon positions. Marked excesses of transitions over chance expectation are seen for the third positions of proteincoding genes and for the gene for the small subunit of ribosomal RNA. For the third codon positions the excess of transitions is adequately explained as due to therestriction of observable substitutions to transitions for conserved amino acids with two-codon families; the excessof transitions over expectation forthe small ribosomal subunit suggests that theconservation of nucleotide size is favored by selection.

NIMAL mitochondrial DNA (mtDNA) occursas a single circular molecule, generally about 16,000 bp long. This organelle genome contains 13 (orsometimes 12"WOLSTENHOLME et al. 1987; OKIMOTO et al. 1992) protein-encoding genes, the genes for 22 tRNAs and two ribosomal RNA subunits, and a noncoding region containing the origin of replication for the heavy strand in vertebrates (BROWN 1985) and both strandsin Drosophila (CLARY WOLSTENand HOLME 1987). Other than this latter control region, noncodingnucleotides arerare in animal mtDNA (HARRISON1989). Gene order variation occurs between both and within phyla. Among vertebrates, birds differ from mammals and amphibians in gene order, suggesting that the move of a segment containingone tRNA and one protein-encoding gene occurred in the ancestor of class Aves (DESJARDINS MORAIS1990). Within and
The sequence data presented in this article have been submitted to the EMBL/GenBank Data Librariesunder the accession number L06178. Genetics 133: 97-1 17 Uanuary, 1993)

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mammals, marsupials differfromeutherians in the positions of some tRNAs (PAABo et al. 1991). Within insects, tRNAgenes are known to vary in position both between the orders Diptera (CLARY and WOLSTENHOLME 1985) and Hymenoptera (CROZIER, CROZIER and MACKINLAY1989) and within theorder Diptera, with differences...