Transcriptome Profiling of Starvation in the Peripheral Chemosensory Organs of the Crop Pest Spodoptera littoralis Caterpillars

Starvation is frequently encountered by animals under fluctuating food conditions in nature, and response to it is vital for life span. Many studies have investigated the behavioral and physiological responses to starvation. In particular, starvation is known to induce changes in olfactory behaviors and olfactory sensitivity to food odorants, but the underlying mechanisms are not well understood. Here, we investigated the transcriptional changes induced by starvation in the chemosensory tissues of the caterpillar Spodoptera littoralis, using Illumina RNA sequencing. Gene expression profiling revealed 81 regulated transcripts associated with several biological processes, such as glucose metabolism, immune defense, response to stress, foraging activity, and olfaction. Focusing on the olfactory process, we observed changes in transcripts encoding proteins putatively involved in the peri-receptor events, namely, chemosensory proteins and odorant-degrading enzymes. Such modulation of their expression may drive fluctuations in the dynamics and the sensitivity of the olfactory receptor neuron response. In combination with the enhanced presynaptic activity mediated via the short neuropeptide F expressed during fasting periods, this could explain an enhanced olfactory detection process. Our observations suggest that a coordinated transcriptional response of peripheral chemosensory organs participates in the regulation of olfactory signal reception and olfactory-driven behaviors upon starvation.

G protein-coupled receptors as candidates for modulation and activation of the chemical senses in decapod crustaceans

Many studies have characterized class A GPCRs in crustaceans; however, their expression in crustacean chemosensory organs has yet to be detailed. Class A GPCRs comprise several subclasses mediating diverse functions. In this study, using sequence homology, we classified all putative class A GPCRs in two chemosensory organs (antennular lateral flagellum [LF] and walking leg dactyls) and brain of four species of decapod crustaceans (Caribbean spiny lobster Panulirus argus, American lobster Homarus americanus, red-swamp crayfish Procambarus clarkii, and blue crab Callinectes sapidus). We identified 333 putative class A GPCRs– 83 from P. argus, 81 from H. americanus, 102 from P. clarkii, and 67 from C. sapidus–which belong to five distinct subclasses. The numbers of sequences for each subclass in the four decapod species are (in parentheses): opsins (19), small-molecule receptors including biogenic amine receptors (83), neuropeptide receptors (90), leucine-rich repeat-containing GPCRs (LGRs) (24), orphan receptors (117). Most class A GPCRs are predominately expressed in the brain; however, we identified multiple transcripts enriched in the LF and several in the dactyl. In total, we found 55 sequences with higher expression in the chemosensory organs relative to the brain across three decapod species. We also identified novel transcripts enriched in the LF including a metabotropic histamine receptor and numerous orphan receptors. Our work establishes expression patterns for class A GPCRs in the chemosensory organs of crustaceans, providing insight into molecular mechanisms mediating neurotransmission, neuromodulation, and possibly chemoreception.

Lipocalins in arthropod chemical communication

Lipocalins represent one of the most successful superfamilies of proteins. Most of them are extracellular carriers for hydrophobic ligands across aqueous media, but other functions have been reported. They are present in most living organisms including bacteria. In animals they have been identified in mammals, molluscs and arthropods; sequences have also been reported for plants. A sub-group of lipocalins, referred to as odorant-binding proteins (OBPs), mediate chemical communication in mammals by ferrying specific pheromones to the vomeronasal organ. So far, these proteins have not been reported as carriers of semiochemicals in other living organisms; instead chemical communication in arthropods is mediated by other protein families structurally unrelated to lipocalins. A search in the databases has revealed extensive duplication and differentiation of lipocalin genes in some species of insects, crustaceans and chelicerates. Their large numbers, ranging from a handful to few dozens in the same species, their wide divergence, both within and between species, and their expression in chemosensory organs suggest that such expansion may have occurred under environmental pressure, thus supporting the hypothesis that lipocalins may be involved in chemical communication in arthropods.

The 40-Year Mystery of Insect Odorant-Binding Proteins

The survival of insects depends on their ability to detect molecules present in their environment. Odorant-binding proteins (OBPs) form a family of proteins involved in chemoreception. While OBPs were initially found in olfactory appendages, recently these proteins were discovered in other chemosensory and non-chemosensory organs. OBPs can bind, solubilize and transport hydrophobic stimuli to chemoreceptors across the aqueous sensilla lymph. In addition to this broadly accepted “transporter role”, OBPs can also buffer sudden changes in odorant levels and are involved in hygro-reception. The physiological roles of OBPs expressed in other body tissues, such as mouthparts, pheromone glands, reproductive organs, digestive tract and venom glands, remain to be investigated. This review provides an updated panorama on the varied structural aspects, binding properties, tissue expression and functional roles of insect OBPs.

The Effects of Population Density on the Incidence of Developmental Deformities in Chemosensory Organs of Tobacco Hornworm Larvae (Lepidoptera: Sphingidae)

Cultures of Manduca sexta Johanssen in our laboratory were found to have larvae with missing or deformed mouthparts or antennae. Hypothesizing that these developmental deformities were caused by crowded rearing conditions, we reared larvae in four different population densities and recorded the incidence (% of larvae affected) and types of chemoreceptor deformities. Results showed that the incidence of these deformities was directly proportional to larval population density. Deformities of the maxilla and palp were the most frequent, followed by those of the antenna, epipharynx and maxillary styloconica. Life history traits of larval mass, food consumption, and rate of development were inversely related to larval density for both normal and deformed larvae. We discuss possible causes and mechanisms of these deformities and of changes to life history traits.

Functional integration of “undead” neurons in the olfactory system

Programmed cell death (PCD) is widespread during neurodevelopment, eliminating the surpluses of neuronal production. Using the Drosophila olfactory system, we examined the potential of cells fated to die to contribute to circuit evolution. Inhibition of PCD is sufficient to generate new cells that express neural markers and exhibit odor-evoked activity. These “undead” neurons express a subset of olfactory receptors that is enriched for relatively recent receptor duplicates and includes some normally found in different chemosensory organs and life stages. Moreover, undead neuron axons integrate into the olfactory circuitry in the brain, forming novel receptor/glomerular couplings. Comparison of homologous olfactory lineages across drosophilids reveals natural examples of fate change from death to a functional neuron. Last, we provide evidence that PCD contributes to evolutionary differences in carbon dioxide–sensing circuit formation in Drosophila and mosquitoes. These results reveal the remarkable potential of alterations in PCD patterning to evolve new neural pathways.

Functional integration of “undead” neurons in the olfactory system

ABSTRACTProgrammed cell death (PCD) is widespread during neurodevelopment, typically eliminating the surpluses of neuronal production. Employing the Drosophila olfactory system, we examined the potential of cells fated to die to contribute to circuit evolution. Inhibition of PCD is sufficient to generate many new cells that express neural markers and exhibit odor-evoked activity. These “undead” neurons express a subset of olfactory receptors that, intriguingly, is enriched for recent receptor duplicates and include some normally found in other chemosensory organs and life-stages. Moreover, undead neuron axons integrate into the olfactory circuitry in the brain, forming novel receptor/glomerular couplings. Comparison of homologous olfactory lineages across drosophilids reveals natural examples of fate changes from death to a functional neuron. Finally, we provide evidence that PCD contributes to evolutionary differences in carbon dioxide-sensing circuit formation in Drosophila and mosquitoes. These results reveal the remarkable potential of alterations in PCD patterning to evolve new neural pathways.