Expression map of a complete set of gustatory receptor genes in chemosensory organs of Bombyx mori

Abstract

Most lepidopteran species are herbivores, and interaction with host plants affects their gene expression and behavior as well as their genome evolution. Gustatory receptors (Grs) are expected to mediate host plant selection, feeding, oviposition and courtship behavior. However, due to their high diversity, sequence divergence and extremely low level of expression it has been difficult to identify precisely a complete set of Grs in Lepidoptera. By manual annotation and BAC sequencing, we improved annotation of 43 gene sequences compared with previously reported Grs in the most studied lepidopteran model, the silkworm, Bombyx mori, and identified 7 new tandem copies of BmGr30 on chromosome 7, bringing the total number of BmGrs to 76. Among these, we mapped 68 genes to chromosomes in a newly constructed chromosome distribution map and 8 genes to scaffolds; we also found new evidence for large clusters of BmGrs, especially from the bitter receptor family. RNA-seq analysis of diverse BmGr expression patterns in chemosensory organs of larvae and adults enabled us to draw a precise organ specific map of BmGr expression. Interestingly, most of the clustered genes were expressed in the same tissues and more than half of the genes were expressed in larval maxillae, larval thoracic legs and adult legs. For example, BmGr63 showed high expression levels in all organs in both larval and adult stages. By contrast, some genes showed expression limited to specific developmental stages or organs and tissues. BmGr19 was highly expressed in larval chemosensory organs (especially antennae and thoracic legs), the single exon genes BmGr53 and BmGr67 were expressed exclusively in larval tissues, the BmGr27-BmGr31 gene cluster on chr7 displayed a high expression level limited to adult legs and the candidate CO receptor BmGr2 was highly expressed in adult antennae, where few other Grs were expressed. Transcriptional analysis of the Grs in B. mori provides a valuable new reference for finding genes involved in plant-insect interactions in Lepidoptera and establishing correlations between these genes and vital insect behaviors like host plant selection and courtship for mating.

Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest

“…GRs, especially, are highly variable among species, which could be a major factor for host plant adaptation. GRs are categorized into three classes-CO 2 receptors, sugar receptors and bitter receptors-among which bitter receptors are most variable, while CO 2 and sugar receptors are conserved [14][15][16][17][18] . Manual annotation identified 237 GR genes in the S. litura genome ( Table 2, Fig.…”

“…Manual annotation identified 237 GR genes in the S. litura genome ( Table 2, Fig. 1a and Supplementary Table 13), whereas in the other lepidopteran species investigated to date, most of which are mono-and oligophagous, only about GRs are reported 8,11,14,16,19,20 . Since large expansions of GR genes were also reported recently in S. frugiperda 5 and in another polyphagous noctuid, Helicoverpa armigera 21 , the expansion of GRs may be a unique adaptation mechanism for polyphagous Noctuidae to feed on a wide variety of host plants (Table 2).…”

“…Recently, the role of SlituCYP321b1 in insecticide resistance was confirmed by showing that it is overexpressed in the midgut after induction by several pesticides, and that RNAimediated silencing of SlituCYP321b1 significantly increased mortality of S. litura larvae exposed to the same pesticides 27 . Thirteen bitter GR genes clustered on S. litura Chr 14 were mainly expressed in moth proboscis and larval maxilla, whereas the corresponding BmorGR gene cluster on Chr 10 composed of BmorGR55-57 was expressed in larval chemoreception organs 16 . c, Expansion of S. litura single-exon bitter GR genes on Chr 25 mainly expressed in moth proboscis.…”

Changes in the Peripheral Chemosensory System Drive Adaptive Shifts in Food Preferences in Insects

“…Genomic and bioinformatic analyses of GR organization in holometabolous insects, including Diptera (Clyne et al, 2000; Scott et al, 2001; Hill et al, 2002; Robertson et al, 2003; Kent et al, 2008), Coleoptera (McKenna et al, 2016), Lepidoptera (Guo et al, 2017), and Hymenoptera (Robertson and Wanner, 2006) characterized 68 putatively functional GRs in D. melanogaster , 76 in the African malaria mosquito ( Anopheles gambiae ), 91 in the yellow fever mosquito ( Aedes aegypti ), 222 in the red flour beetle ( Tribolium castaneum ), 234 in the Asian longhorned beetle ( Anoplophora glabripennis ), 76 in the silkmoth ( Bombyx mori ), 5 in the fig wasp ( Ceratosolen solmsi ), and 12 in the European honey bee ( Apis mellifera ). The Drosophila GRs are functionally categorized for CO 2 detection, sugar and amino acid detection (sweet), noxious substance detection (bitter) and pheromone detection.…”

Contact chemosensation of phytochemicals by insect herbivores

“…6,37,38 A GR expressed in the larval stage may not be expressed in the adult stage and vice versa , which likely reflects the variety of host plant species and thus phytochemicals encountered throughout development. For example, in many lepidopteran species, larvae are leaf-feeding, whereas adults are nectar-feeding.…”