Characteristics of the nuclear (18S, 5.8S, 28S, and 5S) and mitochondrial (16S and 12S) rDNA genes of Apis mellifera (Insecta: Hymenoptera): Structure, organization, and retrotransposition.
Joseph J. Gillespie 1,2,3*, J. Spencer Johnston 1, Jamie J. Cannone 4, Thomas H. Eickbush 5, Robin R. Gutell 4
1 Department of Entomology, Texas A&M University, College Station, TX 77843, USA
2 Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA
3 Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, VA 24061, USA
4 Institute for Cellular and Molecular Biology and Section of Integrative Biology, University of Texas, Austin, TX 78712, USA
5 Department of Biology, University of Rochester, Rochester, NY 14627, USA
As an accompanying manuscript to the release of the honeybee genome, we report the entire sequence of the nuclear (18S, 5.8S, 28S, and 5S) and mitochondrial (16S and 12S) ribosomal RNA (rRNA)-encoding gene sequences (rDNA) and related internally and externally transcribed spacer regions of Apis mellifera (Insecta: Hymenoptera: Apocrita). Additionally, we predict secondary structures for the mature rRNA molecules based on comparative sequence analyses with other arthropod taxa and reference to recently published crystalline structures of the ribosome. In general, the structure of honeybee rRNAs are in agreement with previously predicted rRNA models from other arthropods in core regions of the rRNA, with little expansion in non-conserved regions. Our multiple sequence alignments are made available on several public databases and provide a preliminary establishment of a global structural model of all rRNAs from the insects. Additionally, we provide conserved stretches of sequences flanking the rDNA cistrons that comprise the externally transcribed spacer regions (ETS) and part of the intergenic spacer region (IGS), including several repetitive motifs. Finally, we report the occurrence of retrotransposition in the nuclear large subunit rDNA, as R2 elements are present in the usual insertion points found in other arthropods. Interestingly, functional R1 elements, also usually present in the genomes of insects, were not detected in the honeybee rDNA genes. The reverse transcriptase products of the R2 elements are deduced from their putative open reading frames and structurally aligned with those from another hymenopteran insect, the jewel wasp Nasonia (Pteromalidae). Stretches of conserved amino acids shared between Apis and Nasonia are illustrated and serve as potential sites for primer design, as target amplicons within these R2 elements may serve as novel phylogenetic markers for Hymenoptera. Given the impending completion of the sequencing of the Nasonia genome, we expect our report to eventually shed light on the evolution of the hymenopteran genome within higher insects, particularly regarding the relative maintenance of conserved rDNA genes, related variable spacer regions, and retrotransposable elements.
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