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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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A novel exon in BmGr5-8. The amino acids of the TM5 and TM6 regions encoded by the ends of the exons flanking the novel exon are shown aligned with each other for the seven moth SRs. Amino acids shared by at least six of the sequences are highlighted in bold font. Like other SRs, BmGr4 does not have the novel exon, and the same is predicted for HvCr1. The location of the phase 2 intron in BmGr4 (intron p in Figure 6) is shown. BmGr5-8 have a short novel exon encoding 15–20 unconserved amino acids, and an additional flanking phase 2 intron (intron q in Figure 6). HvCr5 is predicted to have an intron q, however the precise location cannot be predicted.
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Figure 5: A novel exon in BmGr5-8. The amino acids of the TM5 and TM6 regions encoded by the ends of the exons flanking the novel exon are shown aligned with each other for the seven moth SRs. Amino acids shared by at least six of the sequences are highlighted in bold font. Like other SRs, BmGr4 does not have the novel exon, and the same is predicted for HvCr1. The location of the phase 2 intron in BmGr4 (intron p in Figure 6) is shown. BmGr5-8 have a short novel exon encoding 15–20 unconserved amino acids, and an additional flanking phase 2 intron (intron q in Figure 6). HvCr5 is predicted to have an intron q, however the precise location cannot be predicted.

Mentions: Krieger et al. [24] included cDNA sequences for two SRs in their initial description of a set of candidate chemoreceptors from the noctuid moth Heliothis virescens based on private partial genome sequences generated by Bayer and Exelixis Corporations. They subsequently obtained cDNAs, called Cr1 and Cr5 in their publication, which turn out to represent two divergent SR lineages within moths, as revealed by examination of the Gr family in the genome of the silkmoth Bombyx mori [25,26]. Details of our analysis of the Gr family in B. mori are published elsewhere [15], but we include the five SRs here for completeness. B. mori has a single ortholog of HvCr5, which we have named BmGr4 (BmGr1-3 are the carbon dioxide receptors [27]). B. mori also has a simple ortholog of HvCr1, named BmGr6, as well as an expansion of three other genes, BmGr5, BmGr7, and BmGr8, in a monophyletic lineage with HvCr1/BmGr6. The monophyly of this lineage is supported not only by bootstrapping, but by each member's (BmGr5-8 and we predict HvCr1 as well) remarkable possession of a newly evolved short exon from within the ancestral phase 2 intron p (see intron details below). This novel exon is supported by a partial cDNA sequence for BmGr6, which was submitted to GenBank as "candidate olfactory receptor BmOR20" [GenBank:BAF31192.1 by T. Sakusai, Y. Hashimoto, and T. Nishioka in 2006], but which has a deletion of an upstream exon preventing complete translation. It has also been confirmed by sequencing of an RT/PCR product between the flanking exons for BmGr8 [15]; [GenBank:EU769119], and is inferred bioinformatically for BmGr5 and BmGr7. It encodes 15–20 amino acids in BmGr5-8 (Figure 5), and at least that number of amino acids in HvCr1 (where the genome sequence is not available, but the cDNA encodes these extra amino acids). These amino acids show no sequence conservation and are part of the extracellular loop 3 (ECL3; see below). This loop is usually very short in all insect Grs, so this evolution of a novel exon encoding a short stretch of variable amino acids that lengthen ECL3 is unusual.


Evolution of the sugar receptors in insects.

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

A novel exon in BmGr5-8. The amino acids of the TM5 and TM6 regions encoded by the ends of the exons flanking the novel exon are shown aligned with each other for the seven moth SRs. Amino acids shared by at least six of the sequences are highlighted in bold font. Like other SRs, BmGr4 does not have the novel exon, and the same is predicted for HvCr1. The location of the phase 2 intron in BmGr4 (intron p in Figure 6) is shown. BmGr5-8 have a short novel exon encoding 15–20 unconserved amino acids, and an additional flanking phase 2 intron (intron q in Figure 6). HvCr5 is predicted to have an intron q, however the precise location cannot be predicted.
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Figure 5: A novel exon in BmGr5-8. The amino acids of the TM5 and TM6 regions encoded by the ends of the exons flanking the novel exon are shown aligned with each other for the seven moth SRs. Amino acids shared by at least six of the sequences are highlighted in bold font. Like other SRs, BmGr4 does not have the novel exon, and the same is predicted for HvCr1. The location of the phase 2 intron in BmGr4 (intron p in Figure 6) is shown. BmGr5-8 have a short novel exon encoding 15–20 unconserved amino acids, and an additional flanking phase 2 intron (intron q in Figure 6). HvCr5 is predicted to have an intron q, however the precise location cannot be predicted.
Mentions: Krieger et al. [24] included cDNA sequences for two SRs in their initial description of a set of candidate chemoreceptors from the noctuid moth Heliothis virescens based on private partial genome sequences generated by Bayer and Exelixis Corporations. They subsequently obtained cDNAs, called Cr1 and Cr5 in their publication, which turn out to represent two divergent SR lineages within moths, as revealed by examination of the Gr family in the genome of the silkmoth Bombyx mori [25,26]. Details of our analysis of the Gr family in B. mori are published elsewhere [15], but we include the five SRs here for completeness. B. mori has a single ortholog of HvCr5, which we have named BmGr4 (BmGr1-3 are the carbon dioxide receptors [27]). B. mori also has a simple ortholog of HvCr1, named BmGr6, as well as an expansion of three other genes, BmGr5, BmGr7, and BmGr8, in a monophyletic lineage with HvCr1/BmGr6. The monophyly of this lineage is supported not only by bootstrapping, but by each member's (BmGr5-8 and we predict HvCr1 as well) remarkable possession of a newly evolved short exon from within the ancestral phase 2 intron p (see intron details below). This novel exon is supported by a partial cDNA sequence for BmGr6, which was submitted to GenBank as "candidate olfactory receptor BmOR20" [GenBank:BAF31192.1 by T. Sakusai, Y. Hashimoto, and T. Nishioka in 2006], but which has a deletion of an upstream exon preventing complete translation. It has also been confirmed by sequencing of an RT/PCR product between the flanking exons for BmGr8 [15]; [GenBank:EU769119], and is inferred bioinformatically for BmGr5 and BmGr7. It encodes 15–20 amino acids in BmGr5-8 (Figure 5), and at least that number of amino acids in HvCr1 (where the genome sequence is not available, but the cDNA encodes these extra amino acids). These amino acids show no sequence conservation and are part of the extracellular loop 3 (ECL3; see below). This loop is usually very short in all insect Grs, so this evolution of a novel exon encoding a short stretch of variable amino acids that lengthen ECL3 is unusual.

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