Odorant Binding Proteins of the Red Imported Fire Ant, Solenopsis invicta: An Example of the Problems Facing the Analysis of Widely Divergent Proteins

Gotzek, Dietrich; Robertson, Hugh M.; Wurm, Yannick; Shoemaker, DeWayne

doi:10.1371/journal.pone.0016289

Cited by 46 publications

(62 citation statements)

References 67 publications

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“…In contrast to previous hypotheses [17, 18], it is primarily a conserved subset of single-copy orthologs which are expressed in ant antennae. In Cerapachys biroi , only one dynamically evolving CSP is expressed specifically in antennae, in contrast to five conserved OBPs and two conserved CSPs showing antenna-specific expression.…”

Section: Discussioncontrasting

confidence: 68%

Comparative genomics and transcriptomics in ants provide new insights into the evolution and function of odorant binding and chemosensory proteins

2014

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BackgroundThe complex societies of ants and other social insects rely on sophisticated chemical communication. Two families of small soluble proteins, the odorant binding and chemosensory proteins (OBPs and CSPs), are believed to be important in insect chemosensation. To better understand the role of these proteins in ant olfaction, we examined their evolution and expression across the ants using phylogenetics and sex- and tissue-specific RNA-seq.ResultsWe find that subsets of both OBPs and CSPs are expressed in the antennae, contradicting the previous hypothesis that CSPs have replaced OBPs in ant olfaction. Both protein families have several highly conserved clades with a single ortholog in all eusocial hymenopterans, as well as clades with more dynamic evolution and many taxon-specific radiations. The dynamically evolving OBPs and CSPs have been hypothesized to function in chemical communication. Intriguingly, we find that seven members of the conserved clades are expressed specifically in the antennae of the clonal raider ant Cerapachys biroi, whereas only one dynamically evolving CSP is antenna specific. The orthologs of the conserved, antenna-specific C. biroi genes are also expressed in antennae of the ants Camponotus floridanus and Harpegnathos saltator, indicating that antenna-specific expression of these OBPs and CSPs is conserved across ants. Most members of the dynamically evolving clades in both protein families are expressed primarily in non-chemosensory tissues and thus likely do not fulfill chemosensory functions.ConclusionsOur results identify candidate OBPs and CSPs that are likely involved in conserved aspects of ant olfaction, and suggest that OBPs and CSPs may not rapidly evolve to recognize species-specific signals.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-718) contains supplementary material, which is available to authorized users.

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Section: Discussioncontrasting

confidence: 68%

Comparative genomics and transcriptomics in ants provide new insights into the evolution and function of odorant binding and chemosensory proteins

2014

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“…Similarly, jewel wasps have 90 OBPs, while honeybees (with 21) and fire ants (with 18) have far fewer [30], and fig wasps have just seven. The contrast with other herbivorous insects is also striking.…”

Section: Resultsmentioning

confidence: 99%

Obligate mutualism within a host drives the extreme specialization of a fig wasp genome

et al. 2013

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BackgroundFig pollinating wasps form obligate symbioses with their fig hosts. This mutualism arose approximately 75 million years ago. Unlike many other intimate symbioses, which involve vertical transmission of symbionts to host offspring, female fig wasps fly great distances to transfer horizontally between hosts. In contrast, male wasps are wingless and cannot disperse. Symbionts that keep intimate contact with their hosts often show genome reduction, but it is not clear if the wide dispersal of female fig wasps will counteract this general tendency. We sequenced the genome of the fig wasp Ceratosolen solmsi to address this question.ResultsThe genome size of the fig wasp C. solmsi is typical of insects, but has undergone dramatic reductions of gene families involved in environmental sensing and detoxification. The streamlined chemosensory ability reflects the overwhelming importance of females finding trees of their only host species, Ficus hispida, during their fleeting adult lives. Despite long-distance dispersal, little need exists for detoxification or environmental protection because fig wasps spend nearly all of their lives inside a largely benign host. Analyses of transcriptomes in females and males at four key life stages reveal that the extreme anatomical sexual dimorphism of fig wasps may result from a strong bias in sex-differential gene expression.ConclusionsOur comparison of the C. solmsi genome with other insects provides new insights into the evolution of obligate mutualism. The draft genome of the fig wasp, and transcriptomic comparisons between both sexes at four different life stages, provide insights into the molecular basis for the extreme anatomical sexual dimorphism of this species.

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“…CSPs (17,18). Because ants detect a large variety of chemicals derived from their habitats by chemosensory receptors, they require unidentified carrier protein(s) with a flexible structure that can bind various semiochemicals with moderate selectivity.…”

Section: Significancementioning

confidence: 99%

Niemann–Pick type C2 protein mediating chemical communication in the worker ant

Ishida

Tsuchiya

Fujii

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

104

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Ants are eusocial insects that are found in most regions of the world. Within its caste, worker ants are responsible for various tasks that are required for colony maintenance. In their chemical communication, α-helical carrier proteins, odorant-binding proteins, and chemosensory proteins, which accumulate in the sensillum lymph in the antennae, play essential roles in transferring hydrophobic semiochemicals to chemosensory receptors. It has been hypothesized that semiochemicals are recognized by α-helical carrier proteins. The number of these proteins, however, is not sufficient to interact with a large number of semiochemicals estimated from chemosensory receptor genes. Here we shed light on this conundrum by identifying a Niemann–Pick type C2 (NPC2) protein from the antenna of the worker Japanese carpenter ant, Camponotus japonicus (CjapNPC2). CjapNPC2 accumulated in the sensillum cavity in the basiconic sensillum. The ligand-binding pocket of CjapNPC2 was composed of a flexible β-structure that allowed it to bind to a wide range of potential semiochemicals. Some of the semiochemicals elicited electrophysiolgical responses in the worker antenna. In vertebrates, NPC2 acts as an essential carrier protein for cholesterol from late endosomes and lysosomes to other cellular organelles. However, the ants have evolved an NPC2 with a malleable ligand-binding pocket as a moderately selective carrier protein in the sensillum cavity of the basiconic sensillum. CjapNPC2 might be able to deliver various hydrophobic semiochemicals to chemosensory receptor neurons and plays crucial roles in chemical communication required to perform the worker ant tasks.

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Odorant Binding Proteins of the Red Imported Fire Ant, Solenopsis invicta: An Example of the Problems Facing the Analysis of Widely Divergent Proteins

Cited by 46 publications

References 67 publications

Comparative genomics and transcriptomics in ants provide new insights into the evolution and function of odorant binding and chemosensory proteins

Comparative genomics and transcriptomics in ants provide new insights into the evolution and function of odorant binding and chemosensory proteins

Obligate mutualism within a host drives the extreme specialization of a fig wasp genome

Niemann–Pick type C2 protein mediating chemical communication in the worker ant

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