The Molecular Basis of Host Selection in a Crucifer-Specialized Moth

Liu, Xiaolong; Zhang, J.; Yan, Qi; Miao, Chun-Li; Han, Wei‐Kang; Hou, Wen; Yang, Ke; Hansson, Bill S.; Peng, Yajun; Guo, Jin‐Meng; Xu, Hao; Wang, Chen-Zhu; Dong, Shuang-Lin; Knaden, Markus

doi:10.1016/j.cub.2020.08.047

Cited by 68 publications

(69 citation statements)

References 31 publications

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“…3A, B). Remarkably, these two compounds have been identified in various Brassicales plants, including A. thaliana (Liu et al, 2020). Thus, these results suggest that these two ITC compounds may also be important for host-plant selection in S. flava, and in Brassicales specialists from other orders.…”

Section: S Flava Or67b Triplication Resulted In Paralogs With Distinct But Overlapping Itc Selectivitymentioning

confidence: 66%

“…Apart from the ITC-sensitive Ors described here, a recent study in the moth Plutella xylostella, also a specialist of Brassicales plants, reported two Ors (Or35 and Or49) that are also selective for ITCs and important for oviposition (Liu et al, 2020). As mentioned above, it is relevant that these Ors are selective to three ITC compounds including two (3MPITC and PITC) that activate S. flava Or67b paralogs strongly.…”

Section: An Olfactory Receptor Sensitive To a New Niche-specific Chemical Class Of Odorant Compoundsmentioning

confidence: 53%

“…Interestingly, both BITC and 3MIPTC (iberverin) activated all S. flava paralogs at all concentrations (with the exception of Sfla Or67b2 at the lowest concentration of BITC; Figure 4B). Of particular significance is that in the specialist moth Plutella xyllostella, 3MPITC was also recently reported to activate ITC-selective Ors and to stimulate oviposition (Liu et al, 2020). PITC has similar physiological and behavioral effects in this moth species, and in S. flava it selectively activates Or67b3 across the range of concentrations tested (Fig.…”

Section: S Flava Or67b Triplication Resulted In Paralogs With Distinct But Overlapping Itc Selectivitymentioning

confidence: 77%

“…OSNs expressing Dmel Or67b respond strongly to stimulation with apple cider vinegar (Figure 2), a potent Drosophila attractant (Liu et al, 2020;Figure 5), which collectively suggests that the Or67b circuit mediates behavioral attraction. Finally, D. mojavensis OSNs expressing Or67b detect aromatic volatile compounds from its cacti hosts (Crowley-Gall et al, 2016;Date et al, 2013).…”

Section: An Olfactory Receptor Mediating Attraction To Mustard Host Plantsmentioning

confidence: 88%

“…However, the evolutionary mechanisms underlying the chemosensory adaptations to these toxic plants are generally unknown in herbivorous insects (Liu et al, 2020). Identifying these mechanisms can help us understand the evolution of extant herbivorous insect species, 90% of which are specialized on a limited set of toxic host plants (Bernays and Graham 1988).…”

Section: Introductionmentioning

confidence: 99%

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Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

Matsunaga

Reisenman

Goldman-Huertas

et al. 2019

Preprint

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248): 21 Plant toxins are effective defenses because they are aversive to most insects. The same 22 molecules, however, are co-opted as host-finding cues by specialist herbivores. Although such 23 behavioral shifts are central to our understanding of herbivorous insect diversification, it is not 24 well understood how these behaviors evolve. We addressed this in Scaptomyza flava, a 25 herbivorous drosophilid fly within a lineage that shifted to feeding on toxic mustard plants 26 (Brassicales) less than 10 million years ago. S flava lost the ancestral attraction to yeast volatiles 27 and the attendant chemoreceptors used to detect these odors. Here we report that S. flava, but not 28 its close microbe-feeding relatives Drosophila melanogaster and S. pallida, is attracted to 29 mustard host-plant odors, including volatile mustard oils (isothiocyanates or ITCs). Our genomic 30 analysis uncovered three S. flava paralogs of an olfactory receptor gene (Or67b) that likely 31 experienced recent positive selection. We then tested whether these chemoreceptors could 32 underlie the observed attraction to volatile ITCs. Our in vivo recordings revealed that two of the 33 S. flava Or67b proteins (Or67b1 and Or67b3) -but not the homologous Ors from microbe-34 feeding relatives -responded selectively and sensitively to volatile ITCs. These Ors are the first 35 ITC chemoreceptors other than TRP channel family (e.g., the TrpA1 'wasabi' receptor) known 36 from any animal. Remarkably, S. flava Or67b3 was sufficient to drive olfactory attraction toward 37 butyl ITC when expressed in an attractive olfactory circuit. Our study illuminates that ancestrally 38 aversive chemicals can be co-opted as attractants through gene duplication, leading to the origin 39 of hedonic valence shifts in herbivorous insects. 40 41 42Significance Statement (120) 43 Plant toxins trigger aversive olfactory (volatile-mediated) and gustatory (contact-mediated) 44 responses in animals. Paradoxically, toxic plants are often colonized by specialist insects that co-45 opt these toxins as host-plant finding cues. The mechanisms underlying these behavioral shifts, 46 from indifference or repulsion to plant chemicals, to attraction, remain unclear. To address this, 47 we used a fly lineage, Scaptomyza, that switched from yeast-feeding to feeding on mustard plants 48 less than 10 million years ago. We found that S. flava is attracted to mustard-plant odors and 49 volatile mustard oils (isothiocyanates or ITCs) such as 'wasabi', a behavior enabled by the 50 evolution of genes encoding odorant receptors highly sensitive to ITCs. Our study illuminates 51 how insects colonize toxic host plants through duplication and ecological repurposing of genes 52 encoding pre-existing chemoreceptors. 53 54 55 56 57 Many plant compounds used in food, agriculture and medicine originally evolved as 58 toxins that deter and repel enemies (1). Among the most well-known compounds are those 59 reactive electrophiles that induce the sensation of pain, such as diallyl disulfide a...

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Section: S Flava Or67b Triplication Resulted In Paralogs With Distinct But Overlapping Itc Selectivitymentioning

confidence: 66%

Section: An Olfactory Receptor Sensitive To a New Niche-specific Chemical Class Of Odorant Compoundsmentioning

confidence: 53%

Section: S Flava Or67b Triplication Resulted In Paralogs With Distinct But Overlapping Itc Selectivitymentioning

confidence: 77%

Section: An Olfactory Receptor Mediating Attraction To Mustard Host Plantsmentioning

confidence: 88%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

Matsunaga

Reisenman

Goldman-Huertas

et al. 2019

Preprint

View full text Add to dashboard Cite

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Molecular mechanism of sex pheromone perception in male Mythimna loreyi revealed by in vitro system

Zhang,

Bai,

Guo

et al. 2023

Pest Management Science

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BACKGROUNDMythimna loreyi is an important agricultural pest with a sensitive sex pheromone communication system. To clarify the pheromone binding proteins (PBPs) and pheromone receptors (PRs) involved in sex pheromone perception is important for both understanding the molecular olfactory mechanism and developing a new pest control strategy in M. loreyi.RESULTSFirst, the electroantennogram (EAG) assay showed that male M. loreyi displayed the highest response to the major sex pheromone component Z9‐14:Ac, and higher responses to two minor components, Z7‐12:Ac and Z11‐16:Ac. Second, the fluorescence competition binding assay showed that PBP1 bound all three pheromones and other tested compounds with high or moderate affinity, while PBP2 and PBP3 each bound only one pheromone component and few other compounds. Third, functional study using the Xenopus oocyte system demonstrated that, of the six candidate PRs, PR2 was weakly sensitive to the major pheromone Z9‐14:Ac, but was strongly sensitive to pheromone analog Z9‐14:OH; PR3 was strongly and specifically sensitive to a minor component Z7‐12:Ac; PR4 and OR33 were both weakly sensitive to another minor component, Z11‐16:Ac. Finally, phylogenetic relationship and ligand profiles of PRs were compared among six species from two closely related genera Mythimna and Spodoptera, suggesting functional shifts of M. loreyi PRs toward Spodoptera PRs.CONCLUSIONFunctional differentiations were revealed among three PBPs and six PRs in sex pheromone perception, laying an important basis for understanding the molecular mechanism of sex pheromone perception and for developing new control strategies in M. loreyi. © 2023 Society of Chemical Industry.

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Does fungal infection increase the palatability of oilseed rape to insects?

Jindřichová,

Rubil,

Rezek

et al. 2024

Pest Management Science

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BACKGROUNDMultiple and simultaneous attacks by pathogens and insect pests frequently occur in nature. Plants respond to biotic stresses by activating distinct defense mechanisms, but little is known about how plants cope with multiple stresses. The focus of this study was the combined interaction of fungal infection caused by Leptosphaeria maculans (synonym Plenodomus lingam) and arthropod infestation by the diamondback moth (Plutella xylostella) in oilseed rape (Brassica napus). We hypothesized that infection by the fungal pathogen L. maculans could alter oilseed rape palatability to P. xylostella‐chewing caterpillars. Feeding preference tests were complemented with analyses of defense gene transcription, and levels of glucosinolates (GLSs) and volatile organic compounds (VOCs) in L. maculans‐inoculated and non‐inoculated (control) leaves to determine possible causes of larval choice.RESULTSCaterpillars preferred true leaves to cotyledons, hence true leaves were used for further experiments. True leaves inoculated with L. maculans were more palatable to caterpillars over control leaves during the early stage of infection at 3 days post inoculation (dpi), but this preference disappeared in the later stages of infection at 7 dpi. In parallel, genes involved in the salicylic acid and ethylene pathways were up‐regulated in L. maculans‐inoculated leaves at 3 and 7 dpi; L. maculans increased the level of total aliphatic GLSs, specifically glucobrassicanapin, and decreased the level of glucoiberin at 3 dpi and altered the content of specific VOCs. A group of 55 VOCs with the highest variability between treatments was identified.CONCLUSIONWe suggest that the P. xylostella preference for L. maculans‐inoculated leaves in the early stage of disease development could be caused by the underlying mechanisms leading to changes in metabolic composition. Further research should pinpoint the compounds responsible for driving larval preference and evaluate whether the behavior of the adult moths, i.e. the stage that makes the first choice regarding host plant selection in field conditions, correlates with our results on larval host acceptance. © 2024 Society of Chemical Industry.

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The Molecular Basis of Host Selection in a Crucifer-Specialized Moth

Cited by 68 publications

References 31 publications

Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

Molecular mechanism of sex pheromone perception in male Mythimna loreyi revealed by in vitro system

Does fungal infection increase the palatability of oilseed rape to insects?

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