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Evolution of the sugar receptors in insects.

Kent LB, Robertson HM - BMC Evol. Biol. (2009)

Bottom Line: Twelve intron gains and 63 losses are inferred within the SR family.Examination of the SRs in these fly, mosquito, moth, beetle, and hymenopteran genome sequences reveals that they appear to have originated independently from single ancestral genes within the dipteran and coleopteran lineages, and two genes in the lepidopteran and hymenopteran lineages.The origin of the insect SRs will eventually be illuminated by additional basal insect and arthropod genome sequences.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Entomology, University of Illinois at Urbana-Champaign, 61801, USA. lkent@life.uiuc.edu

ABSTRACT

Background: Perception of sugars is an invaluable ability for insects which often derive quickly accessible energy from these molecules. A distinctive subfamily of eight proteins within the gustatory receptor (Gr) family has been identified as sugar receptors (SRs) in Drosophila melanogaster (Gr5a, Gr61a, and Gr64a-f). We examined the evolution of these SRs within the 12 available Drosophila genome sequences, as well as three mosquito, two moth, and beetle, bee, and wasp genome sequences.

Results: While most Drosophila species retain all eight genes, we find that the three Drosophila subgenus species have lost Gr64d, while D. grimshawi and the D. pseudoobscura/persimilis sibling species have also lost Gr5a function. The entire Gr64 gene complex was also duplicated in the D. grimshawi lineage, but only one potentially functional copy of each gene has been retained. The numbers of SRs range from two in the hymenopterans Apis mellifera and Nasonia vitripennis to 16 in the beetle Tribolium castaneum. An unusual aspect is the evolution of a novel exon from intronic sequence in an expanded set of four SRs in Bombyx mori (BmGr5-8), which appears to be the first example of such exonization in insects. Twelve intron gains and 63 losses are inferred within the SR family.

Conclusion: Examination of the SRs in these fly, mosquito, moth, beetle, and hymenopteran genome sequences reveals that they appear to have originated independently from single ancestral genes within the dipteran and coleopteran lineages, and two genes in the lepidopteran and hymenopteran lineages. The origin of the insect SRs will eventually be illuminated by additional basal insect and arthropod genome sequences.

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Schematic diagram of the two SR gene complexes in D. grimshawi. The two complexes and their genes are labeled 1 and 2 for the centromeric and telomeric complexes, with intact genes shown as solid boxes, pseudogenes as grey boxes, and pseudogenic gene fragments as short grey boxes. Direction of transcription is shown by arrow heads. Paralogy is indicated by dashed lines. Not to scale.
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Figure 2: Schematic diagram of the two SR gene complexes in D. grimshawi. The two complexes and their genes are labeled 1 and 2 for the centromeric and telomeric complexes, with intact genes shown as solid boxes, pseudogenes as grey boxes, and pseudogenic gene fragments as short grey boxes. Direction of transcription is shown by arrow heads. Paralogy is indicated by dashed lines. Not to scale.

Mentions: For the most part the 12 available Drosophila genome sequences contain single intact orthologs for each of the eight Drosophila SR lineages (Figure 1). The only previously known exception is that Gr5a is missing from D. pseudoobscura [9,19] and, not surprisingly, its sibling species D. persimilis. There are, however, several other instances of gene subfamily evolution within this fly genus. Gr64e appears to be a pseudogene in both of these species because the intron donor splice site on the penultimate intron starts with GA instead of the canonical GT. Gr5a is a severely damaged pseudogene in the Hawaiian D. grimshawi, and is not included in the tree analysis. In addition, there was a duplication of the entire 3rd chromosome gene complex in D. grimshawi, roughly 2.6 Mbp apart, followed by the loss or pseudogenization of each gene in one or the other version of the complex, leaving a single intact copy of each gene (Figure 2). Thus the centromeric complex retains a functional copy of Gr61a, a pseudogenic copy of Gr64a, and functional copies of Gr64b, Gr64c, and Gr64e, followed by a fragment of Gr64f, while the telomeric complex has an intact copy of Gr64a and Gr64f, and fragments of Gr61a, Gr64b, Gr64c, and Gr64e. We designate genes in the centromeric complex by the number "1" after their name and the telomeric complex by the number "2". In addition, Gr64d is missing from the three Drosophila subgenus species, D. virilis, D. mojavensis, and D. grimshawi, so this loss predates the duplication of the complex in the D. grimshawi lineage. Judging from the branch lengths of the DgriGr64a1P/2 copies, this gene complex duplication is relatively old and may be present in all Hawaiian Drosophila. We have not determined how extensive the duplication is, but it presumably involves multiple flanking genes as well. Another slightly unusual problem is the phylogenetic placement of what we are calling Gr64d in D. willistoni. This gene is in the expected location for Gr64d, that is between Gr64c and Gr64e, however phylogenetically it is clearly closer to the Gr64c genes than the Gr64d genes. There is no simple explanation for this situation. A duplication of Gr64c in D. willistoni followed by loss of the original Gr64d gene should lead to our Gr64d clustering with the D. willistoni Gr64c, and there is no evidence of a partial gene conversion event. We are also able to date roughly the movement of Gr5a and Gr61a from the tandem complex of Gr64a-f. All Drosophila species appear to have Gr5a on their X chromosomes, so this gene relocation predates the genus. However, Gr61a is located in inverse orientation at the 5' end of the complex, in all species up to D. ananassae, so it must have relocated thereafter. Finally, Gr61a is relocated to the X chromosome in D. yakuba. The result is that the number of apparently intact SRs in these 12 Drosophila species is six in D. pseudoobscura/persimilis and D. grimshawi, seven in D. virilis and D. mojavensis, and eight in the remainder of the species.


Evolution of the sugar receptors in insects.

Kent LB, Robertson HM - BMC Evol. Biol. (2009)

Schematic diagram of the two SR gene complexes in D. grimshawi. The two complexes and their genes are labeled 1 and 2 for the centromeric and telomeric complexes, with intact genes shown as solid boxes, pseudogenes as grey boxes, and pseudogenic gene fragments as short grey boxes. Direction of transcription is shown by arrow heads. Paralogy is indicated by dashed lines. Not to scale.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2667405&req=5

Figure 2: Schematic diagram of the two SR gene complexes in D. grimshawi. The two complexes and their genes are labeled 1 and 2 for the centromeric and telomeric complexes, with intact genes shown as solid boxes, pseudogenes as grey boxes, and pseudogenic gene fragments as short grey boxes. Direction of transcription is shown by arrow heads. Paralogy is indicated by dashed lines. Not to scale.
Mentions: For the most part the 12 available Drosophila genome sequences contain single intact orthologs for each of the eight Drosophila SR lineages (Figure 1). The only previously known exception is that Gr5a is missing from D. pseudoobscura [9,19] and, not surprisingly, its sibling species D. persimilis. There are, however, several other instances of gene subfamily evolution within this fly genus. Gr64e appears to be a pseudogene in both of these species because the intron donor splice site on the penultimate intron starts with GA instead of the canonical GT. Gr5a is a severely damaged pseudogene in the Hawaiian D. grimshawi, and is not included in the tree analysis. In addition, there was a duplication of the entire 3rd chromosome gene complex in D. grimshawi, roughly 2.6 Mbp apart, followed by the loss or pseudogenization of each gene in one or the other version of the complex, leaving a single intact copy of each gene (Figure 2). Thus the centromeric complex retains a functional copy of Gr61a, a pseudogenic copy of Gr64a, and functional copies of Gr64b, Gr64c, and Gr64e, followed by a fragment of Gr64f, while the telomeric complex has an intact copy of Gr64a and Gr64f, and fragments of Gr61a, Gr64b, Gr64c, and Gr64e. We designate genes in the centromeric complex by the number "1" after their name and the telomeric complex by the number "2". In addition, Gr64d is missing from the three Drosophila subgenus species, D. virilis, D. mojavensis, and D. grimshawi, so this loss predates the duplication of the complex in the D. grimshawi lineage. Judging from the branch lengths of the DgriGr64a1P/2 copies, this gene complex duplication is relatively old and may be present in all Hawaiian Drosophila. We have not determined how extensive the duplication is, but it presumably involves multiple flanking genes as well. Another slightly unusual problem is the phylogenetic placement of what we are calling Gr64d in D. willistoni. This gene is in the expected location for Gr64d, that is between Gr64c and Gr64e, however phylogenetically it is clearly closer to the Gr64c genes than the Gr64d genes. There is no simple explanation for this situation. A duplication of Gr64c in D. willistoni followed by loss of the original Gr64d gene should lead to our Gr64d clustering with the D. willistoni Gr64c, and there is no evidence of a partial gene conversion event. We are also able to date roughly the movement of Gr5a and Gr61a from the tandem complex of Gr64a-f. All Drosophila species appear to have Gr5a on their X chromosomes, so this gene relocation predates the genus. However, Gr61a is located in inverse orientation at the 5' end of the complex, in all species up to D. ananassae, so it must have relocated thereafter. Finally, Gr61a is relocated to the X chromosome in D. yakuba. The result is that the number of apparently intact SRs in these 12 Drosophila species is six in D. pseudoobscura/persimilis and D. grimshawi, seven in D. virilis and D. mojavensis, and eight in the remainder of the species.

Bottom Line: Twelve intron gains and 63 losses are inferred within the SR family.Examination of the SRs in these fly, mosquito, moth, beetle, and hymenopteran genome sequences reveals that they appear to have originated independently from single ancestral genes within the dipteran and coleopteran lineages, and two genes in the lepidopteran and hymenopteran lineages.The origin of the insect SRs will eventually be illuminated by additional basal insect and arthropod genome sequences.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Entomology, University of Illinois at Urbana-Champaign, 61801, USA. lkent@life.uiuc.edu

ABSTRACT

Background: Perception of sugars is an invaluable ability for insects which often derive quickly accessible energy from these molecules. A distinctive subfamily of eight proteins within the gustatory receptor (Gr) family has been identified as sugar receptors (SRs) in Drosophila melanogaster (Gr5a, Gr61a, and Gr64a-f). We examined the evolution of these SRs within the 12 available Drosophila genome sequences, as well as three mosquito, two moth, and beetle, bee, and wasp genome sequences.

Results: While most Drosophila species retain all eight genes, we find that the three Drosophila subgenus species have lost Gr64d, while D. grimshawi and the D. pseudoobscura/persimilis sibling species have also lost Gr5a function. The entire Gr64 gene complex was also duplicated in the D. grimshawi lineage, but only one potentially functional copy of each gene has been retained. The numbers of SRs range from two in the hymenopterans Apis mellifera and Nasonia vitripennis to 16 in the beetle Tribolium castaneum. An unusual aspect is the evolution of a novel exon from intronic sequence in an expanded set of four SRs in Bombyx mori (BmGr5-8), which appears to be the first example of such exonization in insects. Twelve intron gains and 63 losses are inferred within the SR family.

Conclusion: Examination of the SRs in these fly, mosquito, moth, beetle, and hymenopteran genome sequences reveals that they appear to have originated independently from single ancestral genes within the dipteran and coleopteran lineages, and two genes in the lepidopteran and hymenopteran lineages. The origin of the insect SRs will eventually be illuminated by additional basal insect and arthropod genome sequences.

Show MeSH