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.

Functional odor classification through a medicinal chemistry approach.

Crucial for any hypothesis about odor coding is the classification and prediction of sensory qualities in chemical compounds. The relationship between perceptual quality and molecular structure has occupied olfactory scientists throughout the 20th century, but details of the mechanism remain elusive. Odor molecules are typically organic compounds of low molecular weight that may be aliphatic or aromatic, may be saturated or unsaturated, and may have diverse functional polar groups. However, many molecules conforming to these characteristics are odorless. One approach recently used to solve this problem was to apply machine learning strategies to a large set of odors and human classifiers in an attempt to find common and unique chemical features that would predict a chemical's odor. We use an alternative method that relies more on the biological responses of olfactory sensory neurons and then applies the principles of medicinal chemistry, a technique widely used in drug discovery. We demonstrate the effectiveness of this strategy through a classification for esters, an important odorant for the creation of flavor in wine. Our findings indicate that computational approaches that do not account for biological responses will be plagued by both false positives and false negatives and fail to provide meaningful mechanistic data. However, the two approaches used in tandem could resolve many of the paradoxes in odor perception.

Applying medicinal chemistry strategies to understand odorant discrimination.

Associating an odorant's chemical structure with its percept is a long-standing challenge. One hindrance may come from the adoption of the organic chemistry scheme of molecular description and classification. Chemists classify molecules according to characteristics that are useful in synthesis or isolation, but which may be of little importance to a biological sensory system. Accordingly, we look to medicinal chemistry, which emphasizes biological function over chemical form, in an attempt to discern which among the many molecular features are most important for odour discrimination. Here we use medicinal chemistry concepts to assemble a panel of molecules to test how heteroaromatic ring substitution of the benzene ring will change the odour percept of acetophenone. This work allows us to describe an extensive rule in odorant detection by mammalian olfactory receptors. Whereas organic chemistry would have predicted the ring size and composition to be key features, our work reveals that the topological polar surface area is the key feature for the discrimination of these odorants.

Candidate chemosensory genes in the Stemborer Sesamia nonagrioides.

The stemborer Sesamia nonagrioides is an important pest of maize in the Mediterranean Basin. Like other moths, this noctuid uses its chemosensory system to efficiently interact with its environment. However, very little is known on the molecular mechanisms that underlie chemosensation in this species. Here, we used next-generation sequencing (454 and Illumina) on different tissues from adult and larvae, including chemosensory organs and female ovipositors, to describe the chemosensory transcriptome of S. nonagrioides and identify key molecular components of the pheromone production and detection systems. We identified a total of 68 candidate chemosensory genes in this species, including 31 candidate binding-proteins and 23 chemosensory receptors. In particular, we retrieved the three co-receptors Orco, IR25a and IR8a necessary for chemosensory receptor functioning. Focusing on the pheromonal communication system, we identified a new pheromone-binding protein in this species, four candidate pheromone receptors and 12 carboxylesterases as candidate acetate degrading enzymes. In addition, we identified enzymes putatively involved in S. nonagrioides pheromone biosynthesis, including a ∆11-desaturase and different acetyltransferases and reductases. RNAseq analyses and RT-PCR were combined to profile gene expression in different tissues. This study constitutes the first large scale description of chemosensory genes in S. nonagrioides.

A comparison of the olfactory gene repertoires of adults and larvae in the noctuid moth Spodoptera littoralis.

To better understand the olfactory mechanisms in a lepidopteran pest model species, the cotton leafworm Spodoptera littoralis, we have recently established a partial transcriptome from adult antennae. Here, we completed this transcriptome using next generation sequencing technologies, namely 454 and Illumina, on both adult antennae and larval tissues, including caterpillar antennae and maxillary palps. All sequences were assembled in 77,643 contigs. Their analysis greatly enriched the repertoire of chemosensory genes in this species, with a total of 57 candidate odorant-binding and chemosensory proteins, 47 olfactory receptors, 6 gustatory receptors and 17 ionotropic receptors. Using RT-PCR, we conducted the first exhaustive comparison of olfactory gene expression between larvae and adults in a lepidopteran species. All the 127 candidate olfactory genes were profiled for expression in male and female adult antennae and in caterpillar antennae and maxillary palps. We found that caterpillars expressed a smaller set of olfactory genes than adults, with a large overlap between these two developmental stages. Two binding proteins appeared to be larvae-specific and two others were adult-specific. Interestingly, comparison between caterpillar antennae and maxillary palps revealed numerous organ-specific transcripts, suggesting the complementary involvement of these two organs in larval chemosensory detection. Adult males and females shared the same set of olfactory transcripts, except two male-specific candidate pheromone receptors, two male-specific and two female-specific odorant-binding proteins. This study identified transcripts that may be important for sex-specific or developmental stage-specific chemosensory behaviors.

The use of the sex pheromone as an evolutionary solution to food source selection in caterpillars.

Sex pheromones are released by adults of a species to elicit a sexual interaction with the other sex of the same species. Here we report an unexpected effect of a moth sex pheromone on the caterpillars of the same species. We demonstrate that larvae of the cotton leafworm Spodoptera littoralis are attracted by the moth sex pheromone and that this phenomenon is independent of sex determination. In addition, we show that the olfactory sensilla carried by the caterpillar antennae are sensitive to the pheromone and that the caterpillar sensilla express pheromone-binding proteins that are used by adult antennae to bind pheromone components. Finally, we demonstrate that the larvae are preferentially attracted to a food source when it contains the sex pheromone main component. A possible interpretation of these results is that the sex pheromone is used to promote food search in caterpillars, opening potential new routes for insect pest management.