Abstract
Simple SummaryStarvation increases olfactory sensitivity in a manner that enhances the search for food in animals, including insects. However, the molecular mechanisms via which starvation modulates olfactory receptor neuron function are poorly understood. In this study, we sequenced and compared the whole transcriptomes of the main olfactory organs (antennae and palps) of fed and starved caterpillars from the species Spodoptera littoralis. We revealed that transcripts involved in several biological processes are regulated upon starvation. These processes include glucose metabolism, immune defense, foraging activity, and olfaction. In this last process, we evidenced regulation of chemosensory proteins and odorant-degrading enzymes, known to play a role in the dynamics and the sensitivity of the olfactory receptor neuron response. Our results identify new elements in the cascade of olfactory neuron modulation, in addition to insulin, GABA, and short neuropeptide F signaling.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.
Highlights
The sense of smell and food intake are strongly connected in animals
We first investigated the effect of 24 h starvation on the olfactory behavior of fourth instar S. littoralis larvae using a Petri dish assay (Figure 1a)
Behavioral and physiological evidence of an increase in olfactory sensitivity upon starvation has been reported in both vertebrates and insects [4,16,17,20], but the molecular mechanisms leading to this enhanced sensory sensitivity remain elusive
Summary
The sense of smell and food intake are strongly connected in animals. Olfaction is a critical regulator of food-seeking behaviors across species, and food odor alone can trigger behaviors essential for survival [1,2]. Food intake is under the control of two major anorectic hormones, leptin and insulin [5]. These hormones have been shown to regulate olfactory behaviors, targeting both the central and the peripheral olfactory systems [6,7,8]. The nutritional status—satiety or hunger— regulates olfactory sensitivity. Mosquitoes show a decreased attraction toward prey odors [9,10,11], changes in olfactory sensitivity [11], and down-regulation of some chemosensory genes [10,12,13]. Upon starvation, fruit flies exhibit an increase in their behavioral response to different odors including food odors [16,17], a modification in pheromone perception and courtship [18], and a reduced behavioral avoidance to aversive odors [19]
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
