Abstract
Among the butterflies of the genus Papilio (Lepidoptera: Papilionidae), Papilio hospiton (Géné) has a geographical distribution limited to the Mediterranean islands of Sardinia (Italy) and Corsica (France). This is mainly due to the host range that includes only a few plant species of Apiaceae and Rutaceae growing on these islands. In a previous electrophysiological investigation conducted on the maxillary gustatory system of larvae of P. hospiton and its closely phylogenetically related species Papilio machaon, a significantly higher spike activity was shown for the gustatory neurons of lateral and medial styloconic sensilla in P. hospiton when bitter compounds were tested. This effect was possibly correlated to the limited host choice range for P. hospiton. To shed light on the molecular aspects of this phenomenon, we investigated the expression pattern of sensory-related sequences by conducting a transcriptomic analysis from total RNA isolates of P. hospiton larval maxillae. We identified several transcripts that may be involved in taste (one gustatory receptor, one divergent ionotropic receptor, and several transient receptor potential channels, TRPs) as well as transcripts supporting an olfactory function for this appendage, including odorant receptors (ORs), antennal ionotropic receptors (A-IRs), sensory neuron membrane proteins (SNMPs), and odorant-binding proteins (OBPs). We used Human Embryonic Kidney (HEK293A) cells to heterologously express two of the identified receptors, PhospOR1 and PhospPain, together with their orthologs from P. machaon, for functional characterization. While our data suggest no activation of these two receptors by the ligands known so far to activate the electrophysiological response in larval maxillary neurons of Papilio species, nor temperature activation of both Papilio TRPA-channel Painless, they represent the first attempt in connecting neuronal activity with their molecular bases to unravel diet specialization between closely related Papilio species.
Highlights
External chemoreceptors in lepidopteran larvae are located on the antennae, on the maxillae, and in the epipharynx (Dethier and Schoonhoven, 1969; Laue, 2000)
In this work we conducted a transcriptomic analysis of the larval maxillae of P. hospiton, a species endemic of the Mediterranean islands of Corsica and Sardinia that has been used as a model for the comparative analysis of maxilla taste responses due to its strict olygophagy juxtaposed with the relaxed olygophagy of the closerelated species P. machaon (Sollai et al, 2014, 2015, 2018b; Sollai and Crnjar, 2019)
Our study rendered a handful of sequences encoding for putative odorant receptors (ORs), Ionotropic receptors (IRs), a single Gustatory receptors (GRs), Transient receptor potential (TRP) as well as sensory neuron membrane proteins (SNMPs) and odorantbinding proteins (OBPs), which may represent the key genes involved in neuronal functions in the maxillae and constitute the first sensory-related available sequences for this species
Summary
External chemoreceptors in lepidopteran larvae are located on the antennae, on the maxillae, and in the epipharynx (Dethier and Schoonhoven, 1969; Laue, 2000) Together with this last, the maxillae are the main location of the sense of taste and mediate acceptance or rejection of host plants, underlying diet specialization (Schoonhoven and van Loon, 2002). In the model species Bombyx mori, a two-factor host acceptance system has been proposed In this system, while the chemosensory neurons in the maxillary palps are involved in the detection of leaf-surface compounds and in the induction of a test biting, the chemosensory neurons present in the galea are responsible for sensing the toxic compounds in leaf sap generated by test biting, and mediate the following persistent biting (Tsuneto et al, 2020)
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