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

SIMPLE SUMMARY: Starvation 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. ABSTRACT: 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.