No abstract

Many herbivorous insects are mono- or oligophagous, having evolved to select a limited range of host plants. They specifically identify host-plant leaves using their keen sense of taste. Plant secondary metabolites and sugars are thought to be key chemical cues that enable insects to identify host plants and evaluate their quality as food. However, the neuronal and behavioral mechanisms of host-plant recognition are poorly understood. Here, we report a two-factor host acceptance system in larvae of the silkworm Bombyx mori , a specialist on several mulberry species. The first step is controlled by a chemosensory organ, the maxillary palp (MP). During palpation at the leaf edge, the MP detects trace amounts of leaf-surface compounds, which enables host-plant recognition without biting. Chemosensory neurons in the MP are tuned with ultrahigh sensitivity (thresholds of attomolar to femtomolar) to chlorogenic acid (CGA), quercetin glycosides, and β-sitosterol (βsito). Only if these 3 compounds are detected does the larva make a test bite, which is evaluated in the second step. Low-sensitivity neurons in another chemosensory organ, the maxillary galea (MG), mainly detect sucrose in the leaf sap exuded by test biting, allowing larvae to accept the leaf and proceed to persistent biting (feeding). The two-factor host acceptance system reported here may commonly underlie stereotyped feeding behavior in many phytophagous insects and determine their feeding habits.

In this study, we investigated the activation of TRPV1 and TRPA1 by N-acyl homoserine lactones, quorum sensing molecules produced by Gram-negative bacteria, and the inhibitory effect of TRPV1 and TRPA1 by autoinducing peptides, quorum sensing molecules produced by Gram-positive bacteria, using human embryonic kidney 293T cell lines stably expressing human TRPV1 and TRPA1, respectively. As a result, we found that some N-acyl homoserine lactones, such as N-octanoyl-L-homoserine lactone (C8-HSL), N-nonanoyl-L-homoserine lactone (C9-HSL) and N-decanoyl-L-homoserine lactone (C10-HSL) activated both TRPV1 and TRPA1. In addition, we clarified that some N-acyl homoserine lactones, for example, N-3-oxo-dodecanoyl-L-homoserine lactone (3-oxo-C12-HSL) only activated TRPV1, and N-acyl homoserine lactones having saturated short acyl chain, such as N-acetyl-L-homoserine lactone (C2-HSL) and N-butyryl-L-homoserine lactone (C4-HSL) only activated TRPA1, respectively. Furthermore, we found that an autoinducing peptide, simple linear peptide CHWPR, inhibited both TRPV1 and TRPA1, and peptide having thiolactone ring DICNAYF, thiolactone ring were formed between C3 to F7, strongly inhibited only the TRPV1. Although the specificity of TRPV1 and TRPA1 for quorum sensing molecules were different, these data suggest that both TRPV1 and TRPA1 would function as receptors for quorum sensing molecule produced by bacteria.

No abstract

Oligophagous insect herbivores specifically identify host-plant leaves using their keen sense of taste 1 . Plant secondary metabolites and sugars are key chemical cues for insects to identify host plants and evaluate their nutritional value, respectively 2 . However, it is poorly understood how the insect chemosensory system integrates the information from various gustatory inputs. Here we report that a two-step chemosensory system is responsible for host acceptance by larvae of the silkworm Bombyx mori, a specialist for several mulberry species. The first step controlled by a gustatory organ, the maxillary palp (MP), is host-plant recognition during palpation at the leaf edge. Surprisingly, MP detects chlorogenic acid, quercetin glycosides, and β-sitosterol, which stimulate feeding by the silkworm 3-6 , with ultrasensitivity (thresholds of aM to fM). Detecting a mixture of these compounds triggers test biting. The second step is evaluation of the sugar content in the leaf sap exuded by test biting. Low-sensitivity chemosensory neurons in another gustatory organ, the maxillary galea (MG), mainly detect sucrose in the leaf sap exuded by test biting, allowing larvae to accept the leaf and proceed to persistent biting. Our present work shows the behavioral and neuronal basis of host acceptance in the silkworm, mainly driven by six phytochemicals. It also reveals that the ultra-sensitive gustation via MP strictly limits initiation of feeding in the silkworm unless it detects a certain combination of host compounds, suggesting an essential role of MP in hostplant selection. The two-step chemosensory system reported herein may commonly underlie stereotyped feeding behavior in phytophagous insects and determine their feeding habits. MainHost-plant selection by phytophagous insects is dependent on their acceptance or rejection of plants. To clarify the mechanism of host-plant acceptance by silkworm larvae, we observed larval feeding behavior towards a host leaf from white mulberry Morus alba. When a silkworm encounters a leaf, it first palpates the leaf edge using a peripheral gustatory organ known as the maxilla, intermittently bites the edge several times, and finally engages in continuous biting (2-3 times per second) with its head shaking in the dorso-ventral direction along the leaf edge ( Fig. 1a, Supplementary Video 1). The intermittent biting with palpation and the continuous biting with head-moving are termed test biting and persistent biting, respectively 7,8 . We hypothesized that sensing of chemical cues from a M. alba leaf via the maxilla induces test biting because test biting always occurs after palpation with the maxilla. The maxilla consists of the maxillary palp (MP) and maxillary galea (MG) (Fig. 1b). To assess the roles of MP and MG in induction of test biting, we used MP-or MG-ablated larvae. MP-ablated larvae showed palpation, but no test or persistent biting ( Fig. 1c, d, Supplementary Video 2). MG-ablated larvae showed palpation and test biting, and stopped biting within 1 minute, and did not prog...