Evolution of novel sensory organs in fish with legs.

How do animals evolve new traits? Sea robins are fish that possess specialized leg-like appendages used to "walk" along the sea floor. Here, we show that legs are bona fide sense organs that localize buried prey. Legs are covered in sensory papillae that receive dense innervation from touch-sensitive neurons, express non-canonical epithelial taste receptors, and mediate chemical sensitivity that drives predatory digging behavior. A combination of developmental analyses, crosses between species with and without papillae, and interspecies comparisons of sea robins from around the world demonstrate that papillae represent a key evolutionary innovation associated with behavioral niche expansion on the sea floor. These discoveries provide unique insight into how molecular-, cellular-, and tissue-scale adaptations integrate to produce novel organismic traits and behavior.

Transcriptomic and Gene Expression Analysis of Chemosensory Genes from White Grubs of Hylamorpha elegans (Coleoptera: Scarabaeidae), a Subterranean Pest in South America.

Olfaction and gustation processes play key roles in the life cycle of insects, such as finding and accepting food sources, oviposition sites, and mates, among other fundamental aspects of insect development. In this context, chemosensory genes found in sensory organs (e.g., antennae and maxillary palps) are crucial for understanding insect behaviour, particularly the phytophagous behaviour of insect pests that attack economically important crops. An example is the scarab beetle Hylamorpha elegans, which feeds on the roots of several crops important for livestock in its larval stage. In this study, chemosensory gene candidates of H. elegans white grubs identified through the head transcriptome and phylogenetic and tissue-biased gene expression (antennae, head without antennae, and legs) have been reported. Overall, 47 chemosensory genes were identified (2 ORs, 1 GR, 11 IRs, 9 CSPs, and 24 OBPs). Gene expression analysis revealed the predominant presence of IRs in the legs, whereas ORs and the GR were present in the heads and/or antennae. Particularly, HeleOBP9 and HeleCSP2 were significantly expressed in the head but not in the antennae or legs; these and other genes are discussed as potential targets in the context of H. elegans management.

Taste cells expressing Ionotropic Receptor 94e reciprocally impact feeding and egg laying in Drosophila.

Chemosensory cells across the body of Drosophila melanogaster evaluate the environment to prioritize certain behaviors. Previous mapping of gustatory receptor neurons (GRNs) on the fly labellum identified a set of neurons in L-type sensilla that express Ionotropic Receptor 94e (IR94e), but the impact of IR94e GRNs on behavior remains unclear. We used optogenetics and chemogenetics to activate IR94e neurons and found that they drive mild feeding suppression but enhance egg laying. In vivo calcium imaging revealed that IR94e GRNs respond strongly to certain amino acids, including glutamate, and that IR94e plus co-receptors IR25a and IR76b are required for amino acid detection. Furthermore, IR94e mutants show behavioral changes to solutions containing amino acids, including increased consumption and decreased egg laying. Overall, our results suggest that IR94e GRNs on the fly labellum discourage feeding and encourage egg laying as part of an important behavioral switch in response to certain chemical cues.

Intrinsic Molecular Proton Sensitivity Underlies GPR4 Effects on Retrotrapezoid Nucleus Neuronal Activation and CO2-Stimulated Breathing.

An interoceptive homeostatic reflex monitors levels of CO2/H+ to maintain blood gas homeostasis and rapidly regulate tissue acid-base balance by driving lung ventilation and CO2 excretion-this CO2-evoked increase in respiration is the hypercapnic ventilatory reflex (HCVR). Retrotrapezoid nucleus (RTN) neurons provide crucial excitatory drive to downstream respiratory rhythm/pattern-generating circuits, and their activity is directly modulated by changes in CO2/H+ RTN neurons express GPR4 and TASK-2, global deletion of which abrogates CO2/H+ activation of RTN neurons and the HCVR. It has not been determined if the intrinsic pH sensitivity of these proton detectors is required for these effects. We used CRISPR/Cas9 genome editing to generate mice with mutations in either of two pH-sensing histidine residues in GPR4 to determine effects on RTN neuronal CO2/H+ sensitivity and the HCVR. In global GPR4(H81F) and GPR4(H167F) mice, CO2-stimulated breathing and CO2-induced RTN neuronal activation were strongly blunted, with no effect on hypoxia-stimulated breathing. In brainstem slices from GPR4(H81F) mice, peak firing of RTN neurons during bath acidification was significantly reduced compared with GPR4 wild-type mice, and a subpopulation of RTN neurons was rendered pH-insensitive, phenocopying previous results from GPR4-deleted mice. These effects were independent of changes in RTN number/distribution, neuronal excitability or transcript levels for GPR4 and TASK-2. CO2-stimulated breathing was reduced to a similar extent in GPR4(H81F) and TASK-2-deleted mice, with combined mutation yielding no additional deficit in the HCVR. Together, these data demonstrate that the intrinsic pH sensitivity of GPR4 is necessary for full elaboration of the HCVR.

Human Transient Receptor Potential Ankyrin 1 Channel: Structure, Function, and Physiology.

The transient receptor potential ion channel TRPA1 is a Ca2+-permeable nonselective cation channel widely expressed in sensory neurons, but also in many nonneuronal tissues typically possessing barrier functions, such as the skin, joint synoviocytes, cornea, and the respiratory and intestinal tracts. Here, the primary role of TRPA1 is to detect potential danger stimuli that may threaten the tissue homeostasis and the health of the organism. The ability to directly recognize signals of different modalities, including chemical irritants, extreme temperatures, or osmotic changes resides in the characteristic properties of the ion channel protein complex. Recent advances in cryo-electron microscopy have provided an important framework for understanding the molecular basis of TRPA1 function and have suggested novel directions in the search for its pharmacological regulation. This chapter summarizes the current knowledge of human TRPA1 from a structural and functional perspective and discusses the complex allosteric mechanisms of activation and modulation that play important roles under physiological or pathophysiological conditions. In this context, major challenges for future research on TRPA1 are outlined.

Give-and-take of gustation: the interplay between gustatory neurons and taste buds.

Mammalian taste buds are highly regenerative and can restore themselves after normal wear and tear of the lingual epithelium or following physical and chemical insults, including burns, chemotherapy, and nerve injury. This is due to the continual proliferation, differentiation, and maturation of taste progenitor cells, which then must reconnect with peripheral gustatory neurons to relay taste signals to the brain. The turnover and re-establishment of peripheral taste synapses are vital to maintain this complex sensory system. Over the past several decades, the signal transduction and neurotransmitter release mechanisms within taste cells have been well delineated. However, the complex dynamics between synaptic partners in the tongue (taste cell and gustatory neuron) are only partially understood. In this review, we highlight recent findings that have improved our understanding of the mechanisms governing connectivity and signaling within the taste bud and the still-unresolved questions regarding the complex interactions between taste cells and gustatory neurons.

Unraveling the Roles of Neuropeptides in the Chemosensation of the Root-Knot Nematode Meloidogyne javanica.

The identification of novel drug targets in plant-parasitic nematodes (PPNs) is imperative due to the loss of traditional nematicides and a lack of replacements. Chemosensation, which is pivotal for PPNs in locating host roots, has become a focus in nematode behavioral research. However, its underlying molecular basis is still indistinct in such a diverse group of PPNs. To characterize genes participating in chemosensation in the Javanese root-knot nematode Meloidogyne javanica, RNA-sequencing of the second-stage juveniles (J2s) treated with tomato root exudate (TRE) for 1 h and 6 h was performed. Genes related to chemosensation in M. javanica mainly responded to TRE treatment at 1 h. Moreover, a gene ontology (GO) analysis underscored the significance of the neuropeptide G protein-coupled receptor signaling pathway. Consequently, the repertoire of putative neuropeptides in M. javanica, including FMRFamide-like peptides (FLPs), insulin-like peptides (ILPs), and neuropeptide-like peptides (NLPs), were outlined based on a homology analysis. The gene Mjflp-14a, harboring two neuropeptides, was significantly up-regulated at 1 h TRE treatment. Through peptide synthesis and J2 treatment, one of the two neuropeptides (MjFLP-14-2) was proven to influence the J2 chemotaxis towards tomato root tips. Overall, our study reinforces the potential of nematode neuropeptides as novel targets and tools for root-knot nematode control.

Structural basis of ligand specificity and channel activation in an insect gustatory receptor.

Gustatory receptors (GRs) are critical for insect chemosensation and are potential targets for controlling pests and disease vectors, making their structural investigation a vital step toward such applications. We present structures of Bombyx mori Gr9 (BmGr9), a fructose-gated cation channel, in agonist-free and fructose-bound states. BmGr9 forms a tetramer similar to distantly related insect odorant receptors (ORs). Upon fructose binding, BmGr9's channel gate opens through helix S7b movements. In contrast to ORs, BmGr9's ligand-binding pocket, shaped by a kinked helix S4 and a shorter extracellular S3-S4 loop, is larger and solvent accessible in both agonist-free and fructose-bound states. Also, unlike ORs, fructose binding by BmGr9 involves helix S5 and a pocket lined with aromatic and polar residues. Structure-based sequence alignments reveal distinct patterns of ligand-binding pocket residue conservation in GR subfamilies associated with different ligand classes. These data provide insight into the molecular basis of GR ligand specificity and function.

Tastant-receptor interactions: insights from the fruit fly.

Across species, taste provides important chemical information about potential food sources and the surrounding environment. As details about the chemicals and receptors responsible for gustation are discovered, a complex view of the taste system is emerging with significant contributions from research using the fruit fly, Drosophila melanogaster, as a model organism. In this brief review, we summarize recent advances in Drosophila gustation and their relevance to taste research more broadly. Our goal is to highlight the molecular mechanisms underlying the first step of gustatory circuits: ligand-receptor interactions in primary taste cells. After an introduction to the Drosophila taste system and how it encodes the canonical taste modalities sweet, bitter, and salty, we describe recent insights into the complex nature of carboxylic acid and amino acid detection in the context of sour and umami taste, respectively. Our analysis extends to non-canonical taste modalities including metals, fatty acids, and bacterial components, and highlights unexpected receptors and signaling pathways that have recently been identified in Drosophila taste cells. Comparing the intricate molecular and cellular underpinnings of how ligands are detected in vivo in fruit flies reveals both specific and promiscuous receptor selectivity for taste encoding. Throughout this review, we compare and contextualize these Drosophila findings with mammalian research to not only emphasize the conservation of these chemosensory systems, but to demonstrate the power of this model organism in elucidating the neurobiology of taste and feeding.

Copper-Induced Chemosensory Impairment is Reversed by a Short Depuration Period in Northern Clearwater Crayfish (Faxonius propinquus).

Crayfish rely on their chemosensory system for many essential behaviours including finding food, finding mates, and to recognize individuals. Copper can impair chemosensation in crayfish at low concentrations; however, it is not clear if the effect is ameliorated once copper is removed. To better understand the effect of and recovery from copper exposure in crayfish, we exposed Northern clearwater crayfish (Faxonius propinquus) to 31.3 [Formula: see text] copper for 24 h and measured the response of the crayfish to a food cue. The crayfish were then placed into clean water to depurate for an 24 h. The results demonstrated that the crayfish did not respond to a food cue if they had been exposed to copper, but showed a full response after a 24 h recovery period without copper. Higher concentrations of copper have shown a much longer-term effect in rusty crayfish (Faxonius rustics), indicating there is a concentration where the copper is causing longer-term damage instead of just impairing chemosensation. These results highlight the fact that even though contaminants like copper can have profound effects at low concentrations, by removing the contaminants the effect can be ameliorated.