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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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Hydropathy plot and predicted TM domains for AmGr2. Regions of hydrophobic amino acids yield stretches of positive hydropathy, and these are predicted to be TM domains by the ConPredII prediction program (indicated by thick green bars).
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Figure 14: Hydropathy plot and predicted TM domains for AmGr2. Regions of hydrophobic amino acids yield stretches of positive hydropathy, and these are predicted to be TM domains by the ConPredII prediction program (indicated by thick green bars).

Mentions: Recent studies have shown that the insect Ors, while most likely containing seven TM domains, have the opposite membrane topology to that of the G-protein coupled receptors that constitute chemoreceptors in vertebrates and nematodes [30-33]. That is, their N-termini are internal while their C-termini are external. We believe this topology is present throughout the Gr family as well and hence the entire superfamily [27]. These SRs provide a particularly clear illustration of this topology. Examination of the CLUSTALX alignment in Figure 7 shows clearly the relatively long intracellular (IC) loop 2 between TM4 and TM5, and IC3 between TM6 and TM7. Furthermore, these intracellular loops each have several conserved positively charged arginine (R) and lysine (K) residues, in agreement with the "positive inside" rule of von Heijne [34,35]. In contrast, the extracellular loop 3 between TM5 and TM6 is particularly short (except in the lepidopteran lineage with a novel exon), and devoid of conserved positively charged residues. Similar trends apply to the more N-terminal loops. A remaining uncertainty with respect to the membrane topology of these SRs, and Grs in general, is the presence of a "pre-peak" of hydrophobic amino acids that is less evident in the Ors, the only family studied experimentally to date. This pre-peak is around 21 amino acids long, the minimum required for a TM domain. For most of the SRs, it is predicted to be a TM domain by most hydropathy and TM domain prediction programs, as summarized in the ConPredII website [36]. Most of these proteins are predicted to have eight TM domains with the N-terminus external, although the range is from six to nine TM domains (insect chemoreceptor TM domains are seldom as well-defined as those of most other TM proteins, while TM4 is sometimes split into two). An example of these hydropathy plots, predicted TM domains, and predicted topology is shown for AmGr2 in Figures 14 and 15. Further experimental work will be required to resolve this issue, however, it has now been shown that at least the Ors are in fact ligand-gated ion channels [33,37,38], and the same is surely true of these Grs.


Evolution of the sugar receptors in insects.

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

Hydropathy plot and predicted TM domains for AmGr2. Regions of hydrophobic amino acids yield stretches of positive hydropathy, and these are predicted to be TM domains by the ConPredII prediction program (indicated by thick green bars).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 14: Hydropathy plot and predicted TM domains for AmGr2. Regions of hydrophobic amino acids yield stretches of positive hydropathy, and these are predicted to be TM domains by the ConPredII prediction program (indicated by thick green bars).
Mentions: Recent studies have shown that the insect Ors, while most likely containing seven TM domains, have the opposite membrane topology to that of the G-protein coupled receptors that constitute chemoreceptors in vertebrates and nematodes [30-33]. That is, their N-termini are internal while their C-termini are external. We believe this topology is present throughout the Gr family as well and hence the entire superfamily [27]. These SRs provide a particularly clear illustration of this topology. Examination of the CLUSTALX alignment in Figure 7 shows clearly the relatively long intracellular (IC) loop 2 between TM4 and TM5, and IC3 between TM6 and TM7. Furthermore, these intracellular loops each have several conserved positively charged arginine (R) and lysine (K) residues, in agreement with the "positive inside" rule of von Heijne [34,35]. In contrast, the extracellular loop 3 between TM5 and TM6 is particularly short (except in the lepidopteran lineage with a novel exon), and devoid of conserved positively charged residues. Similar trends apply to the more N-terminal loops. A remaining uncertainty with respect to the membrane topology of these SRs, and Grs in general, is the presence of a "pre-peak" of hydrophobic amino acids that is less evident in the Ors, the only family studied experimentally to date. This pre-peak is around 21 amino acids long, the minimum required for a TM domain. For most of the SRs, it is predicted to be a TM domain by most hydropathy and TM domain prediction programs, as summarized in the ConPredII website [36]. Most of these proteins are predicted to have eight TM domains with the N-terminus external, although the range is from six to nine TM domains (insect chemoreceptor TM domains are seldom as well-defined as those of most other TM proteins, while TM4 is sometimes split into two). An example of these hydropathy plots, predicted TM domains, and predicted topology is shown for AmGr2 in Figures 14 and 15. Further experimental work will be required to resolve this issue, however, it has now been shown that at least the Ors are in fact ligand-gated ion channels [33,37,38], and the same is surely true of these Grs.

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
Related in: MedlinePlus