Si-CSP9 regulates the integument and moulting process of larvae in the red imported fire ant, Solenopsis invicta

Cheng, Daifeng; Lu, Yongyue; Ling, Zeng; Liang, Guangwen; Xiao, He

doi:10.1038/srep09245

Cited by 42 publications

(42 citation statements)

References 55 publications

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“…Such a finding has been seen for a number of CSPs, e.g. AmCSP5 and SiCSP9, implicated in mediating embryonic development in A. mellifera and larval molting in S. invicta , respectively 40 41 . It is tempting to speculate that some OBPs act as carriers of developmental signaling molecules and further studies probing such functions are warranted.…”

Section: Discussionsupporting

confidence: 52%

Tissue, developmental, and caste-specific expression of odorant binding proteins in a eusocial insect, the red imported fire ant, Solenopsis invicta

Zhang

Wanchoo

Ortiz‐Urquiza

et al. 2016

Sci Rep

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Insects interact with the surrounding environment via chemoreception, and in social insects such as ants, chemoreception functions to mediate diverse behaviors including food acquisition, self/non-self recognition, and intraspecific communication. The invasive red imported fire ant, Solenopsis invicta, has spread worldwide, displaying a remarkable environmental adaptability. Odorant binding proteins (OBPs) are chemical compound carriers, involved in diverse physiological processes including odor detection and chemical transport. S. invicta contains a highly divergent 17-member OBP gene family, that includes an ant-specific expansion and the social organization implicated Gp-9 (OBP3) gene. A systematic gene expression analysis of the SiOBP repertoire was performed across social caste (workers, male and female alates), tissues (antennae, head, thorax, and abdomen), and developmental stages (egg, larvae, and pupae), revealing that although SiOBPs were expressed in the antennae, the major regions of expression were in the head and thorax across all castes, and the abdomen in male and female alates. SiOBPs were very highly expressed in female alates and at somewhat lower levels in male alates and workers. SiOBPs were differentially expressed, with unique signatures in various castes and tissues, suggesting functionality of SiOBPs beyond olfaction Expression patterns of SiOBP subgroups also showed relationships with their evolutionary relatedness.

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Section: Discussionsupporting

confidence: 52%

Tissue, developmental, and caste-specific expression of odorant binding proteins in a eusocial insect, the red imported fire ant, Solenopsis invicta

Zhang

Wanchoo

Ortiz‐Urquiza

et al. 2016

Sci Rep

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“…The potential functions of OBPs/CSPs in nonantennal body parts are still poorly understood, although there are some data. For example, OBPs have been found associated with leg regeneration in the American cockroach (Kitabayashi, Arai, Kubo, & Natori, ; Nomura, Kawasaki, Kubo, & Natori, ), visual pigment transportation in Lepidoptera (Zhu et al, ), and larval molting in S. invicta (Cheng, Lu, Zeng, Liang, & He, ). Our comparative expression results suggest that SiOBP12b ′ has at least two functions: chemical perception in the antennae and an unknown, possibly ancestral, function in other tissues (e.g., replacement of the degenerated parental SiOBP12 ).…”

Section: Discussionmentioning

confidence: 99%

Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior?

Dang

Cohanim

Fontana

et al. 2019

Ecology and Evolution

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Queen discrimination behavior in the fire ant Solenopsis invicta maintains its two types of societies: colonies with one (monogyne) or many (polygyne) queens, yet the underlying genetic mechanism is poorly understood. This behavior is controlled by two supergene alleles, SB and Sb, with ~600 genes. Polygyne workers, having either the SB/SB or SB/Sb genotype, accept additional SB/Sb queens into their colonies but kill SB/SB queens. In contrast, monogyne workers, all SB/SB, reject all additional queens regardless of genotype. Because the SB and Sb alleles have suppressed recombination, determining which genes within the supergene mediate this differential worker behavior is difficult. We hypothesized that the alternate worker genotypes sense queens differently because of the evolution of differential expression of key genes in their main sensory organ, the antennae. To identify such genes, we sequenced RNA from four replicates of pooled antennae from three classes of workers: monogyne SB/SB, polygyne SB/SB, and polygyne SB/Sb. We identified 81 differentially expressed protein‐coding genes with 13 encoding potential chemical metabolism or perception proteins. We focused on the two odorant perception genes: an odorant receptor SiOR463 and an odorant‐binding protein SiOBP12. We found that SiOR463 has been lost in the Sb genome. In contrast, SiOBP12 has an Sb‐specific duplication, SiOBP12b′, which is expressed in the SB/Sb worker antennae, while both paralogs are expressed in the body. Comparisons with another fire ant species revealed that SiOBP12b′ antennal expression is specific to S. invicta and suggests that queen discrimination may have evolved, in part, through expression neofunctionalization.

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“…Numbers refer to species studied and references, as follows: (1) S podoptera litura (Zhang et al., ); C hilo suppressalis (Xia et al., ); A grotis ipsilon (Gu et al., ); A grotis segetum (Strandh et al., ); S esamia inferens (Zhang et al., ); B ombyx mori (Dani et al., ); (2) A pis mellifera (Iovinella et al., ); (3) L eptopilina heterotoma (Heavner et al., ); P teromalus puparum (Wang et al., ); S irex noctilio (Wang et al., ); A pis mellifera (Li et al., ) (4) D rosophila melanogaster (Dyanov & Dzitoeva, ; Takemori & Yamamoto, ); (5) H elicoverpa armigera (Y.L. Sun et al., 2012 b ); (6) L ocusta migratoria (Ban et al., ; Zhou et al., ); (7) A edes aegypti (Li et al., ; Sirot et al., ); (8) A pis mellifera (Baer et al., ); (9) T ribolium castaneum (Xu et al., ); (10) P eriplaneta americana (Nomura et al., ; Kitabayashi et al., ); (11) A pis mellifera (Maleszka et al., ); (12) S olenopsis invicta (Cheng et al., ); (13) L ocusta migratoria (Guo et al., ); (14) A edes aegypti (Calvo et al., ); A nopheles stephensi (Isawa et al., ); (15) P hormia regina (Ishida et al., ); (16) M amestra brassicae (Nagnan‐Le Meillour et al., ); H elicoverpa armigera (Y.L. Liu et al., 2014 b ; Zhu et al., 2016 a ); (17) H elicoverpa armigera and other species (Zhu et al., 2016 a ); (18) B ombyx mori (Xuan et al., ); (19) B emisia tabaci (G.X.…”

Section: Multiple Functions Of Obps and Cspsmentioning

confidence: 99%

Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects

et al. 2017

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Odorant-binding proteins (OBPs) and chemosensory proteins (CSPs) are regarded as carriers of pheromones and odorants in insect chemoreception. These proteins are typically located in antennae, mouth organs and other chemosensory structures; however, members of both classes of proteins have been detected recently in other parts of the body and various functions have been proposed. The best studied of these non-sensory tasks is performed in pheromone glands, where OBPs and CSPs solubilise hydrophobic semiochemicals and assist their controlled release into the environment. In some cases the same proteins are expressed in antennae and pheromone glands, thus performing a dual role in receiving and broadcasting the same chemical message. Several reports have described OBPs and CSPs in reproductive organs. Some of these proteins are male specific and are transferred to females during mating. They likely carry semiochemicals with different proposed roles, from inhibiting other males from approaching mated females, to marking fertilized eggs, but further experimental evidence is still needed. Before being discovered in insects, the presence of binding proteins in pheromone glands and reproductive organs was widely reported in mammals, where vertebrate OBPs, structurally different from OBPs of insects and belonging to the lipocalin superfamily, are abundant in rodent urine, pig saliva and vaginal discharge of the hamster, as well as in the seminal fluid of rabbits. In at least four cases CSPs have been reported to promote development and regeneration: in embryo maturation in the honeybee, limb regeneration in the cockroach, ecdysis in larvae of fire ants and in promoting phase shift in locusts. Both OBPs and CSPs are also important in nutrition as solubilisers of lipids and other essential components of the diet. Particularly interesting is the affinity for carotenoids of CSPs abundantly secreted in the proboscis of moths and butterflies and the occurrence of the same (or very similar CSPs) in the eyes of the same insects. A role as a carrier of visual pigments for these proteins in insects parallels that of retinol-binding protein in vertebrates, a lipocalin structurally related to OBPs of vertebrates. Other functions of OBPs and CSPs include anti-inflammatory action in haematophagous insects, resistance to insecticides and eggshell formation. Such multiplicity of roles and the high success of both classes of proteins in being adapted to different situations is likely related to their stable scaffolding determining excellent stability to temperature, proteolysis and denaturing agents. The wide versatility of both OBPs and CSPs in nature has suggested several different uses for these proteins in biotechnological applications, from biosensors for odours to scavengers for pollutants and controlled releasers of chemicals in the environment.

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Si-CSP9 regulates the integument and moulting process of larvae in the red imported fire ant, Solenopsis invicta

Cited by 42 publications

References 55 publications

Tissue, developmental, and caste-specific expression of odorant binding proteins in a eusocial insect, the red imported fire ant, Solenopsis invicta

Tissue, developmental, and caste-specific expression of odorant binding proteins in a eusocial insect, the red imported fire ant, Solenopsis invicta

Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior?

Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects

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