Contact chemosensation of phytochemicals by insect herbivores

Pentzold, Stefan; Burse, Antje; Boland, Wilhelm

doi:10.1039/c7np00002b

Cited by 20 publications

(22 citation statements)

References 41 publications

(76 reference statements)

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“…Many herbivorous insects have adapted to a limited range of host plants by overcoming plant defenses against insect herbivory, resulting in mono- and oligophagous insects (so-called specialist insects) [ 1 ]. In parallel, specialists are able to precisely distinguish their host plants from other nonhost plants in their ecosystem using chemical senses, including gustation and olfaction [ 2 ]. In general, gustation is important in determining the acceptance or rejection of a potential food source, whereas olfaction is required when searching for host plants from a distance [ 3 ].…”

Section: Introductionmentioning

confidence: 99%

“…Feeding in insect herbivores is controlled by their physiological responses to phytochemicals that determine the acceptance or rejection of a leaf based on the balance of feeding stimulants and deterrents contained in plant leaves [ 3 , 11 , 12 ]. Chemical ecological studies have identified plant secondary metabolites as feeding stimulants and deterrents for many insect herbivores [ 2 ]. For example, with regard to the silkworm Bombyx mori , a specialist on mulberry leaves, Hamamura and his colleagues identified nonvolatile compounds from mulberry leaves as key signals: isoquercitrin (ISQ) and β-sitosterol (βsito) as biting factors and chlorogenic acid (CGA) as a feeding stimulant that increases feeding amounts in a long-term assay [ 11 , 13 , 14 , 15 ].…”

Section: Introductionmentioning

confidence: 99%

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Diet choice: The two-factor host acceptance system of silkworm larvae

et al. 2020

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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.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Diet choice: The two-factor host acceptance system of silkworm larvae

et al. 2020

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“…Chemosensory proteins (CSPs) are soluble and stable proteins consisting of 6 alphahelices stabilized by two disulphide bonds and a central channel with the capacity to bind small hydrophobic molecules, such as plant volatiles and insect pheromones (1,2). These proteins are often highly expressed in the olfactory and gustatory organs of insects in which they play a role in the sensing of the external environment by carrying volatiles and pheromones to neurons of chemosensilla, leading to downstream behavioural and developmental processes (3,4). For example, CSPs expressed in antenna regulate the transition from solitary to migratory phases of migratory locusts (5), female host-seeking behaviour of tsetse flies (6) and nest mate recognition of ants (2).…”

Section: Introductionmentioning

confidence: 99%

Chemosensory proteins in the CSP4 clade evolved as plant immunity suppressors before two suborders of plant-feeding hemipteran insects diverged

Drurey

Mathers

Prince

et al. 2017

Preprint

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Chemosensory proteins (CSPs) are small globular proteins with hydrophobic binding pockets that have a role in detection of chemicals, regulation of development and growth and host seeking behaviour and feeding of arthropods. Here, we show that a CSP has evolved to modulate plant immune responses. Firstly, we found that the green peach aphid Myzus persicae CSP Mp10, which is delivered into the cytoplasm of plant cells, suppresses the reactive oxygen species (ROS) bursts to both aphid and bacterial elicitors in Arabidopsis thaliana and Nicotiana benthamiana. Aphid RNA interference studies demonstrated that Mp10 modulates the first layer of the plant defence response, specifically the BAK1 pathway.We identified Mp10 homologs in diverse plant-sucking insect species, including aphids, whiteflies, psyllids and leafhoppers, but not in other insect species, including blood-feeding hemipteran insects. We found that Mp10 homologs from other splant-sucking insect species are also capable of suppressing plant ROS. Together, these data and phylogenetic analyses provides evidence that an ancestral Mp10-like sequence acquired plant ROS suppression activity before the divergence of plant-sucking insect species over 250 million years ago. SignificanceAphids, whiteflies, psyllids, leafhoppers and planthoppers are plant-sucking insects of the order Hemiptera that cause dramatic crop losses via direct feeding damage and vectoring of plant pathogens. Chemosensory proteins (CSPs) regulate behavioural and developmental processes in arthropods. Here we show that the CSP Mp10 of the green peach aphid Myzus persicae is an effector that suppresses plant reactive oxygen species (ROS) bursts and the first layer of plant defence responses. Surprisingly, Mp10 homologs are present in diverse plant-feeding hemipteran species, but not blood-feeding ones. An ancestral Mp10-like sequence most likely acquired ROS suppression activity before the divergence of plantsucking insect species 250 million years ago.

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“…Herbivores establish preferences through different types of host-cues (9)(10)(11)(12). Chemical cues, including plant primary and secondary metabolites, are particularly important for herbivores, as they provide specific information about the identity, physiological status and nutritional value of host plants and tissues (13)(14)(15).…”

Section: Introductionmentioning

confidence: 99%

“…Conversely, sugars were found to mask the aversive taste of secondary metabolites (38). Despite these advances, we currently lack a detailed understanding of how primary and secondary metabolites interact to determine herbivore behavior under biologically realistic conditions (9). The paucity of manipulative experiments that test for interactions between host-derived chemical foraging cues in planta limits our capacity to assess the concerted impact of different metabolites on herbivore feeding preferences, and, more generally, our understanding of the role of plant metabolic complexity in herbivore behavior and plant-herbivore interactions.…”

Section: Introductionmentioning

confidence: 99%

Complex plant metabolomes guide fitness-relevant foraging decisions of a specialist herbivore

Machado

Theepan

Robert

et al. 2020

Preprint

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Plants produce complex mixtures of primary and secondary metabolites. Herbivores use these metabolites as behavioral cues to increase their fitness. However, how herbivores integrate primary and secondary metabolites into fitness-relevant foraging decisions in planta is poorly understood. We developed a molecular manipulative approach to modulate the availability of sugars and benzoxazinoid secondary metabolites as foraging cues for a specialist maize herbivore, the western corn rootworm. By disrupting benzoxazinoid biosynthesis in maize and sugar perception in the western corn rootworm, we show that sugars and benzoxazinoids act as distinct and dynamically integrated mediators of short-distance host finding and acceptance. While sugars improve the capacity of rootworm larvae to find a host plant and to distinguish post-embryonic from less nutritious embryonic roots, benzoxazinoids are specifically required for the latter. Host acceptance in the form of root damage is increased by benzoxazinoids and sugars in an additive manner. This pattern is driven by increasing damage to post-embryonic roots in the presence of benzoxazinoids and sugars. Benzoxazinoid- and sugar-mediated foraging directly improves western corn rootworm growth and survival. Interestingly, western corn rootworm larvae retain a substantial fraction of their capacity to feed and survive on maize plants in the absence of both cues. This study unravels fine-grained differentiation and integration of primary and secondary metabolites into herbivore foraging and documents how the capacity to compensate for the absence of important chemical cues enables a specialist herbivore to survive within unpredictable metabolic landscapes.

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Contact chemosensation of phytochemicals by insect herbivores

Abstract: Contact chemosensation, or tasting, enables insect herbivores to identify nonvolatile metabolites in complex mixtures present in plants. The interplay of primary and secondary plant metabolites with gustatory receptors is outlined.

Cited by 20 publications

References 41 publications

Diet choice: The two-factor host acceptance system of silkworm larvae

Diet choice: The two-factor host acceptance system of silkworm larvae

Chemosensory proteins in the CSP4 clade evolved as plant immunity suppressors before two suborders of plant-feeding hemipteran insects diverged

Complex plant metabolomes guide fitness-relevant foraging decisions of a specialist herbivore

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