Spodoptera littoralis genome mining brings insights on the dynamic of expansion of gustatory receptors in polyphagous noctuidae

Abstract

The bitter taste, triggered via gustatory receptors, serves as an important natural defense against the ingestion of poisonous foods in animals, and the increased host breadth is usually linked to an increase in the number of gustatory receptor genes. This has been especially observed in polyphagous insect species, such as noctuid species from the Spodoptera genus. However, the dynamic and physical mechanisms leading to these gene expansions and the evolutionary pressures behind them remain elusive. Among major drivers of genome dynamics are the transposable elements but, surprisingly, their potential role in insect gustatory receptor expansion has not been considered yet. In this work, we hypothesized that transposable elements and possibly positive selection would be involved in the highly dynamic evolution of gustatory receptor in Spodoptera spp. We first sequenced de novo the full 465 Mb genome of S. littoralis, and manually annotated the main chemosensory genes, including a large repertoire of 373 gustatory receptor genes (including 19 pseudogenes). We also improved the completeness of S. frugiperda and S. litura gustatory receptor gene repertoires. Then, we annotated transposable elements and revealed that a particular category of class I retrotransposons, the SINE transposons, was significantly enriched in the vicinity of gustatory receptor gene clusters, suggesting a transposon-mediated mechanism for the formation of these clusters. Selection pressure analyses indicated that positive selection within the gustatory receptor gene family is cryptic, only 7 receptors being identified as positively selected. Altogether, our data provide a new good quality Spodoptera genome, pinpoint interesting gustatory receptor candidates for further functional studies and bring valuable genomic information on the mechanisms of gustatory receptor expansions in polyphagous insect species.

Chromosome‐level genomes of two armyworms, Mythimna separata and Mythimna loreyi, provide insights into the biosynthesis and reception of sex pheromones

“…littoralis expansion of its host range by increasing the number of gustatory receptor copies (Meslin et al, 2022). Our study found that both M. separata and M. loreyi have increased copies of α-amylase, and we hypothesize that transposon expansion and insertion may contribute to their adaptation by enhancing energy metabolism and promoting long-distance migration (Figure 5, Figure S8).…”

The silkworm gustatory receptor BmGr63 is dedicated to the detection of isoquercetin in mulberry

“…The first insect Grs were identified in Drosophila melanogaster [15,16]. Additional Gr data are limited to published genome sequences of particular species including Bombyx mori [17][18][19], Heliconius melpomene [20], Plutella xylostella [21][22][23] and Manduca sexta [24]. Insect Grs often possess seven transmembrane domains with reverse topology when compared with classical G-protein coupled receptors, with an intracellular N-terminus and an extracellular C-terminus [16,18].…”

First chromosome scale genomes of ithomiine butterflies (Nymphalidae: Ithomiini): Comparative models for mimicry genetic studies

“…This high number of genes compared with other Nymphalidae (including D. plexippus ) results from extensive duplications in Ithomiini that occurred in several lineages of the GR phylogeny (Figure 4). So far, such expansions of GR repertoires in Lepidoptera have been documented only in the Noctuidae family, where it has been tentatively linked to polyphagy (Gouin et al, 2017; Meslin et al, 2022). It is interesting to note that somehow similar expansions also occurred independently in Ithomiini, which are not polyphagous but rather oligophagous species (McClure & Elias, 2016b; Willmott & Mallet, 2004).…”

“…For each of the chemosensory gene family, that is, odorant receptors (ORs), the gustatory receptors (GRs), the variant ionotropic receptors (IRs), the odorant‐binding proteins (OBPs) and the chemosensory proteins (CSPs), amino acid sequences previously identified from the genomes of D. plexippus , H. melpomene , S. frugiperda and B. mori (Briscoe et al, 2013; Gouin et al, 2017; Guo et al, 2017; Heliconius Genome Consortium, 2012; Liu et al, 2018; Meslin et al, 2022; Vogt et al, 2015; Zhan et al, 2011) as well as from the transcriptome of M. marsaeus (Piron‐Prunier et al, 2021) were used as queries in a tBLASTn search against genome assemblies of the three species (e‐value threshold 0.001), in order to identify scaffolds containing the genes to annotate. Query amino acid sequences were then aligned on these scaffolds with Exonerate (Slater & Birney, 2005) to identify precise intron‐exon boundaries and create gene models.…”