Evolution of the sugar receptors in insects
© Kent and Robertson; licensee BioMed Central Ltd. 2009
Received: 21 July 2008
Accepted: 18 February 2009
Published: 18 February 2009
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.
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.
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.
Sugars serve as some of the simplest, most easily metabolized forms of energy available to life. For example, despite an anautogenous female mosquito's need for a bloodmeal to nourish her developing eggs, it is the simple nectar of plants that fuels her flight muscles and daily energy needs. As sugar is a valuable resource, it seems fitting that most animals have the ability to taste sugars, and in many it forms a primary stimulatory signal for feeding. The molecular basis for sugar detection in insects has been revealed in Drosophila melanogaster where it involves a series of at least eight genes in the gustatory receptor (Gr) family [1–3]. The first of these is Gr5a on the X chromosome, although identification of this gene as encoding a trehalose receptor was initially confused with the neighboring Tre locus . In phylogenetic analyses, Gr5a clusters with seven other genes on the third chromosome, including the singleton Gr61a and Gr64a-f: six genes in a tandem array , making all of these candidate sugar receptors (SRs). Recent work with these SRs has started to unravel their involvement in sugar detection, although much work remains to understand how these flies perceive sugars. Thorne et al.  and Wang et al.  showed that Gr5a is expressed widely in sensory neurons that detect sugars. Subsequently, Jiao et al.  showed that Gr5a-expressing cells also express undefined combinations of the other seven genes, and showed that Gr64a is required for sensing several sugars other than trehalose. Dahanukar et al.  showed that Gr61a and Gr64f are co-expressed with Gr5a in some but not all sugar-sensitive neurons, indicating that there is a complicated pattern of co-expression of these eight genes. Furthermore, they generated double-mutant flies for both Gr5a and Gr64a that cannot taste any sugars, suggesting that these two receptors co-function with the other six to achieve detection of sugars. Meanwhile, Slone et al.  generated a deletion mutant removing Gr64a-f and found that these flies could not detect most sugars, including trehalose, which is supposed to be detected by Gr5a. Together the evidence from these studies affirms that these eight proteins constitute the SRs in flies, and strongly suggests that they function as heterodimers, perhaps with Gr5a and Gr64a pairing with each other and/or the other less widely-expressed Gr61a and Gr64b-f. Many issues remain unresolved, including the exact ligand specificities of each heterodimeric pair of these eight SRs. Here we contribute to our understanding of these fly SRs by examining their evolution in the 11 newly available Drosophila species genomes , as well as more distant comparisons with the three available mosquito genomes, and the available moth, beetle, bee, and wasp genomes. This analysis reveals an unexpected history of expansion of these gene subfamilies from only one or two genes in each insect order, as well as such unusual features as evolution of a novel exon in a lineage of moth SRs.
Homologs of the eight SR genes in D. melanogaster were identified in the 11 newly available Drosophila species genome sequences using the assemblies available in FlyBase as of October 2007, which are those employed in the genome paper , except that the D. simulans assembly is the "merged" assembly of six different strains. TBLASTN searches were employed to identify these genes, and gene models were constructed using the DmGrs as templates in the text editor of PAUP* v4 . The D. simulans assembly available at FlyBase has numerous problems, including unexplained single base indels relative to the raw traces available in the Trace Archive at the National Center for Biotechnology Information (NCBI). Such errors were present in most of the genes and were corrected.
The mosquito Anopheles gambiae and Aedes aegypti gene models are from Hill et al.  and Kent et al. , but updated in light of gene models constructed for Culex pipiens using the CpipJ1 assembly available at VectorBase, the NCBI, the Broad Institute, and the J. Craig Venter Institute (JCVI). The Bombyx mori moth gene models are from Wanner and Robertson , while those for the red flour beetle Tribolium castaneum were constructed by HMR for the main genome publication . The two honey bee Apis mellifera SRs are from Robertson and Wanner  and their homologs in the parasitoid wasp Nasonia vitripennis were built from the v1.0 assembly available from the Human Genome Sequencing Center at the Baylor College of Medicine and NCBI. The complete set of SRs is provided in a supplementary online FASTA file (Additional file 1).
All proteins were aligned using the multiple alignment program CLUSTALX with default settings . The alignments were used to detect potential problems with the gene models, which were then refined. Phylogenetic analysis was performed using corrected distances, as well as supporting maximum parsimony and maximum likelihood analysis, as described in Robertson et al. , Robertson and Wanner  and Kent et al. . Intron locations and phases were mapped to the protein alignment manually in the PAUP text editor and then mapped to branches in the phylogenetic tree using Dollo parsimony assuming that intron gains are unique but losses are independent events.
The Drosophila SRs
Our analysis of the Drosophila Grs differs somewhat from that recently reported in Gardiner et al. , primarily in that they ignore the Gr5a pseudogene in D. grimshawi, and list multiple copies of Gr61a (5 genes and 3 pseudogenes), Gr64a (4/3), and Gr64b (2/1) in this species beyond what we include (Figure 2). This may be because they used early assemblies from January 2006, which for this species might have had multiple haplotypes alternatively assembled. Remnants of these remain in the October 2007 assemblies as short contigs and were not included in our analysis.
The mosquito SRs
Evolution of the fly SRs
The Tribolium castaneum beetle SRs
The T. castaneum Gr family was described by HMR in the main genome paper , however in the phylogenetic analysis performed therein, the 16 SRs did not cluster as a single lineage, perhaps because the analysis included the entire Gr family. With the current phylogenetic analysis restricted to the SR subfamily, we believe we obtain refined clustering of the Tribolium SRs into a single lineage, however again there is no bootstrap support for this monophyly. Furthermore, we again are not proposing that beetles once had a single SR, simply that the existing Tribolium SR complement of 16 genes is monophyletic. The relatively high divergence of the Tribolium SRs from the other SRs precludes any suggestion of ligand specificity and we propose that all ligand specificity of the Tribolium SRs evolved independently within the beetle lineage.
The moth SRs
The hymenopteran SRs
We examined the newly available parasitoid jewel wasp Nasonia vitripennis genome sequence for SRs, and find only simple orthologs of the Apis mellifera Gr1 and Gr2 genes , sharing 64 and 55 percent sequence identity, respectively (Figure 3). Bees and wasps form a sister group within the order Hymenoptera, so it appears likely that they all have only these two SRs. These two genes are next to and facing each other in a contig of the N. vitripennis genome assembly, but 2 Mbp apart on chromosome 5 in A. mellifera, suggesting that they have remained neighbors in the wasp lineage since their duplication in a common ancestor, but became separated in the bee lineage. These hymenopteran SRs form two sister lineages with the two SR lineages in moths, suggesting that these are rather old gene lineages. Although bootstrap support for this notion is not robust, much like the fly SR lineage sharing the unique intron f, each of these SR lineages in moths and hymenopterans has a unique intron position (g and l, respectively, see below).
We infer 12 intron gains within the SRs (excluding hjmoprs), including the two N-terminal introns (a and b) in the Drosophila Gr5a/Gr64e/Gr64f lineage and mosquito relatives, the splitting of the ancestral phase 2 intron p in the expanded moth SR lineage yielding novel intron q, and eight other novel introns in the non-dipteran genes. Most of these intron locations are not only unique within this SR lineage, but also within the entire Gr family, which represents most of the diversity of the insect chemoreceptor superfamily . Indeed, only the two C-terminal introns r and s (2 and 3 in ) are shared across the Gr family. Intron losses are rather more frequent, totaling 58 in Figure 3, plus seven in the Drosophila species in Figure 1 that do not overlap with Figure 3, for a total of 65. The two C-terminal and ancient introns, r and s, reveal the extremes of intron loss, with intron r being lost 10 times while intron s was only lost twice, in a mosquito lineage and in DwilGr64e. It remains unclear why the final intron is so seldom lost. This pattern is found not only in the SRs, but is consistent throughout the entire superfamily, as this C-terminal intron is almost always present. The only major ambiguity in this analysis of intron evolution is the series of phase 1 introns near the N-terminus, named b, c, and d. These three introns are in roughly the same location, but are found in subsets of the dipteran, moth, and hymenopteran SRs. Unfortunately, the N-terminal sequences are so divergent across these three insect orders that they cannot confidently be considered to be homologous intron placements, and given their disparate locations in the tree, are considered here to be independent gains. As was true for the carbon dioxide receptors , and appears generally true across entire genomes (e.g. ), intron losses are more frequent in the Diptera, with all dipteran gene lineages having lost at least one intron, while some moth, beetle, and hymenopteran lineages have lost none and some only gained introns (although it is also formally possible that some of these non-dipteran introns are ancestral to the SR family and were lost from the dipteran gene lineages).
Distinctive features of SRs
Our analysis of the evolution of the SRs in insects reveals a remarkable pattern (Figure 3). Each major lineage of SRs within an insect order appears to have originated from just one or two genes. Thus we hypothesize that all the fly SRs, all the Tribolium SRs, and most of the moth SRs originated from a single basal gene within each organismal lineage. In contrast, both moths and the hymenopteran wasp/bee lineage appear to have shared two SRs lineages for a long time. Recent work on the SRs in D. melanogaster strongly suggests that, like the Ors and the carbon dioxide receptors, they function as heterodimers [9, 10, 39]. If this is the case, then we can predict that the two existing SRs in the wasp/bee lineage function as a single receptor capable of recognizing all sugars that these hymenopterans can sense. This implies that, much like mammals which have a single heterodimeric SR pair , these species should not be able to differentiate different sugars. We infer then that moths, through duplication of one of their two ancestral SRs into four genes, probably do have the ability to discriminate different sugars, most likely by combining one of these four proteins with the single BmGr4/HvCr5 protein in different gustatory sensory neurons. Finally, although all existing fly and Tribolium SRs each appear to have evolved from a single SR gene, as noted in the results this does not imply that ancestral flies and beetles had a single SR, because additional genes could have been lost. Today, however, flies apparently employ combinations of their SRs allowing recognition and discrimination of diverse sugars. Dahanukar et al.  infer that DmGr5a and DmGr64a are crucial to sugar perception because a double mutant removing both of them is incapable of recognizing any sugars. Since Gr5a and Gr64a are the most widely expressed of the SRs, with Gr61a and Gr64b-f apparently being expressed in limited sets of neurons overlapping with Gr5a and Gr64a [9, 10, 39], a simple model is that functional heterodimers require either Gr5a or Gr64a. An obvious problem with this simple model is that Gr5a has been lost independently from both the D. pseudoobscura/persimilis and D. grimshawi lineages, and it seems unlikely that these species would have lost such a major portion of their sugar-sensing abilities. Gr5a and Gr64a nevertheless do represent the two major SR fly lineages after an initial duplication (Figure 3), so it appears that one daughter gene from each of these two lineages has specialized in being the more widely expressed partner, while the others, Gr61a and Gr64b-f, might be involved in recognition of particular suites of sugars. It is not obvious from the Tribolium SRs which protein(s) might be the widely expressed heterodimeric partner(s) of the others.
An unusual aspect of these SRs is the origin of a novel exon from within an intron in the expanded lineage of moth SRs. Novel exons are known to have evolved from intronic sequences in various vertebrates, in a process called "exonization". Most such instances have resulted from the evolution of splice sites involving a short retrotransposon or SINE, such as Alu elements in humans (reviewed by ), however no such examples appear to have been published from an insect. Exonization is thought to occur with such a retroelement inserted in the opposite orientation to transcription with the inverse "poly-A" tail of the retroelement forming a pseudo 3' splice acceptor site, along with de novo formation of a 5' splice donor site within the retroelement. SINEs are widespread in B. mori [25, 26] and likely other moth genomes, so perhaps such exonization events will be relatively common in moths. This particular event is too old for any vestiges of the potentially originating retroelement to remain. The novel exon in the four BmGr5-8 genes is short, encoding just 15–20 amino acids. The exon exhibits no sequence conservation among the four genes. These extra amino acids nevertheless more than double the length of the third extracellular loop in these four moth SRs relative to all the other SRs, and most other Grs. The origin of the one or two N-terminal exons in the Drosophila Gr5a/64e/f lineage and mosquito relatives, and hence the existence of introns a and b, is also a novelty in the SR subfamily and Gr family, but whether these evolved by insertion of introns into an extended 5' exon, extension of the start of translation into a 5' UTR exon, or true exonization is unclear.
Our investigation reveals that the repertoire of extant insect sugar receptors can be traced to one or two ancestral genes in each major insect order. We are unable to say much about the even older evolutionary history of the insect SRs because the body louse Pediculus humanus, representing a more basal insect lineage in the Exopterygota as compared with the endopterygote insects herein, does not have SRs (HMR unpublished results). The long branch leading to the SRs from the rest of the Gr family , suggests that the louse should have SRs but may have lost them during evolution of its obligate ectoparasitic lifestyle. The imminent availability of genome sequences for two other exopterygote insect lineages, the pea aphid Acyrthosiphon pisum and the kissing bug Rhodnius prolixus, as well as other arthropod genomes, will hopefully further illuminate the origin of the insect sugar receptors from within the Gr family. We predict, however, that those with SRs will always have at least two proteins forming a heterodimer capable of detecting diverse sugars, as represented today by the two SRs in bees and wasps.
This work was supported by NIH grant R01AI56081 and USDA/NRI grant 2007-35604-17756. We thank Kevin Wanner for RT/PCR sequence for BmGr8, Lindy McBride for the DsecGr64f gene sequence, and the Broad Institute and Baylor College of Medicine Genome Sequencing Centers for making the Culex pipiens and Nasonia vitripennis genome assemblies, respectively, available prior to publication.
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