John R. Carlson

Color and scent are well-known pollinator cues. Some plants also produce heat, but its role remains unclear. Here, we report that plant-generated thermal infrared radiation serves as a pollination signal and describe the underlying mechanisms of heat production and infrared detection. Mitochondrial adaptations heat plant reproductive structures in a circadian pattern, radiating infrared that is sufficient to attract beetle pollinators. Beetle antennae contain infrared-activated neurons with thermosensitive ion channels that are structurally tuned to match host plant thermogenesis. Comparative analyses revealed that infrared is among the earliest pollination signals, and indicate a deep-time transition from infrared-based to color-dominated signaling in flowering plants. Our findings uncover an ancient sensory modality shaping the early evolution of pollination, one of the world's most vital processes linking plants and animals.

Chemoreception is the foundation of olfaction and taste, which in insects underlie the detection of humans to which they spread disease and crops that they ravage. Recent advances have provided clear and in some cases surprising new insights into the molecular genetics of chemoreception. We describe mechanisms that govern the choice of a single Odorant receptor (Or) gene by an olfactory receptor neuron (ORN) in Drosophila. We highlight genetic and epigenetic mechanisms by which chemoreceptor expression can be modulated. Exitrons, RNA editing, and pseudo-pseudogenes in chemosensory systems are described. We summarize key insights from the recent structural determinations of odorant and taste receptors. Finally, new molecular components of chemosensory systems, including long non-coding RNAs (lncRNAs), are described.

Summary Identifying a suitable mating partner is an ancient and critical biological problem. How a fruit fly distinguishes a fly of the same species from flies of innumerable related species remains unclear. We analyze the Ir52 receptors, expressed in taste neurons on the fly legs and encoded by a cluster of genes. We find that the cluster shows dynamic evolution, rapidly expanding and contracting over evolutionary time. We develop a novel in vivo expression system and find that Ir52 receptors respond differently to pheromone extracts of different fly species. The receptors are activated by some compounds and inhibited by others, with different receptors showing distinct response profiles. Circuit mapping shows that Ir52 neurons are pre-synaptic to sexually dimorphic neurons that overlap with neurons acting in courtship behavior. Our results support a model in which Ir52 receptors detect information about the species of a potential mating partner.

The taste system controls many insect behaviours, yet little is known about how tastants are encoded in mosquitoes or how they regulate critical behaviours. Here we examine how taste stimuli are encoded by Aedes albopictus mosquitoes—a highly invasive disease vector—and how these cues influence biting, feeding and egg laying. We find that neurons of the labellum, the major taste organ of the head, differentially encode a wide variety of human and other cues. We identify three functional classes of taste sensilla with an expansive coding capacity. In addition to excitatory responses, we identify prevalent inhibitory responses, which are predictive of biting behaviour. Certain bitter compounds suppress physiological and behavioural responses to sugar, suggesting their use as potent stop signals against appetitive cues. Complex cues, including human sweat, nectar and egg-laying site water, elicit distinct response profiles from the neuronal repertoire. We identify key tastants on human skin and in sweat that synergistically promote biting behaviours. Transcriptomic profiling identifies taste receptors that could be targeted to disrupt behaviours. Our study sheds light on key features of the taste system that suggest new ways of manipulating chemosensory function and controlling mosquito vectors. Taste neurons of the mosquito Aedesalbopictus regulate biting, feeding and egg-laying behaviours by responding to taste cues in human sweat, nectar and egg-laying sites via excitation or inhibition.

unveil the structure of a fructose-sensing Gr and provide insight into its function.

Proper expression of odor receptor genes is critical for the function of olfactory systems. In this study, we identified exitrons (exonic introns) in four of the 39 Odorant receptor ( Or ) genes expressed in the Drosophila antenna. Exitrons are sequences that can be spliced out from within a protein-coding exon, thereby altering the encoded protein. We focused on Or88a , which encodes a pheromone receptor, and found that exitron splicing of Or88a is conserved across five Drosophila species over 20 My of evolution. The exitron was spliced out in 15% of Or88a transcripts. Removal of this exitron creates a non-coding RNA rather than an RNA that encodes a stable protein. Our results suggest the hypothesis that in the case of Or88a , exitron splicing could act in neuronal modulation by decreasing the level of functional Or transcripts. Activation of Or88a -expressing olfactory receptor neurons via either optogenetics or pheromone stimulation increased the level of exitron-spliced transcripts, with optogenetic activation leading to a 14-fold increase. A fifth Or can also undergo an alternative splicing event that eliminates most of the canonical open reading frame. Besides these cases of alternative splicing, we found alternative polyadenylation of four Ors , and exposure of Or67c to its ligand ethyl lactate in the antenna downregulated all of its 3′ isoforms. Our study reveals mechanisms by which neuronal activity could be modulated via regulation of the levels of Or isoforms.

Insects taste the external world through taste hairs, or sensilla, that have pores at their tips. When a sensillum comes into contact with a potential food source, compounds from the food source enter through the pore and activate neurons within. For over 50 years, these responses have been recorded using a technique called tip recording. However, this method has major limitations, including the inability to measure neural activity before or after stimulus contact and the requirement for tastants to be soluble in aqueous solutions. We describe here a technique that we call base recording, which overcomes these limitations. Base recording allows the measurement of taste neuron activity before, during, and after the stimulus. Thus, it allows extensive analysis of OFF responses that occur after a taste stimulus. It can be used to study hydrophobic compounds such as long-chain pheromones that have very low solubility in water. In summary, base recording offers the advantages of single-sensillum electrophysiology as a means of measuring neuronal activity - high spatial and temporal resolution, without the need for genetic tools - and overcomes key limitations of the traditional tip recording technique.

Taste systems encode chemical cues that drive vital behaviors. We have elucidated noncanonical features of taste coding using an unconventional kind of electrophysiological analysis. We find that taste neurons of Drosophila are much more sensitive than previously thought. They have a low spontaneous firing frequency that depends on taste receptors. Taste neurons have a dual function as olfactory neurons: They are activated by most tested odorants, including N , N -diethyl- meta -toluamide (DEET), at a distance. DEET can also inhibit certain taste neurons, revealing that there are two modes of taste response: activation and inhibition. We characterize electrophysiological OFF responses and find that the tastants that elicit them are related in structure. OFF responses link tastant identity to behavior: the magnitude of the OFF response elicited by a tastant correlated with the egg laying behavior it elicited. In summary, the sensitivity and coding capacity of the taste system are much greater than previously known.

(Cell Reports 42, 112482; May 30, 2023) Three supplementary figures, Figures S7, S8, and S9C, were incorrectly referred to as Figures S10, S12, and S14, respectively, in the text of the originally published article. The error occurred while reducing the number of supplemental figures to meet the journal requirements. Supplementary File S3 in the original published article used our initial name for new transcripts, “nT,” rather than the name that we finally adopted, “aR,” for antennal transcripts. These errors have been corrected online, and the authors apologize for any confusion that may have been caused. The rich non-coding RNA landscape of the Drosophila antennaTalross et al.Cell ReportsMay 10, 2023In BriefTalross and Carlson generate an atlas of linear and circular lncRNAs in the Drosophila olfactory system. They create an lncRNA-to-neuron map, which shows that olfactory receptor neurons are defined not only by their odor receptors but also by the combination of lncRNAs that they express. Full-Text PDF Open Access

Pain serves critical biological functions, but under some circumstances it is best suppressed. A new study identifies a channel, a neuropeptide, and a pair of neurons in the fly brain that suppress pain.

Emerging evidence suggests that long non-coding RNAs (lncRNAs) play diverse and critical roles in neural development, function, and disease. Here, we examine neuronal lncRNAs in a model system that offers enormous advantages for deciphering their functions: the Drosophila olfactory system. This system is numerically simple, its neurons are exquisitely well defined, and it drives multiple complex behaviors. We undertake a comprehensive survey of linear and circular lncRNAs in the Drosophila antenna and identify a wealth of lncRNAs enriched in it. We generate an unprecedented lncRNA-to-neuron map, which reveals that olfactory receptor neurons are defined not only by their receptors but also by the combination of lncRNAs they express. We identify species-specific lncRNAs, including many that are expressed primarily in pheromone-sensing neurons and that may act in modulation of pheromonal responses or in speciation. This resource opens many new opportunities for investigating the roles of lncRNAs in the nervous system.

Tsetse flies transmit trypanosomes—parasites that cause devastating diseases in humans and livestock—across much of sub-Saharan Africa. Chemical communication through volatile pheromones is common among insects; however, it remains unknown if and how such chemical communication occurs in tsetse flies. We identified methyl palmitoleate (MPO), methyl oleate, and methyl palmitate as compounds that are produced by the tsetse fly Glossina morsitans and elicit strong behavioral responses. MPO evoked a behavioral response in male—but not virgin female— G. morsitans . G. morsitans males mounted females of another species, Glossina fuscipes , when they were treated with MPO. We further identified a subpopulation of olfactory neurons in G. morsitans that increase their firing rate in response to MPO and showed that infecting flies with African trypanosomes alters the flies’ chemical profile and mating behavior. The identification of volatile attractants in tsetse flies may be useful for reducing disease spread.