A heterozygous moth genome provides insights into herbivory and detoxification

Abstract

l e t t e r sHow an insect evolves to become a successful herbivore is of profound biological and practical importance. Herbivores are often adapted to feed on a specific group of evolutionarily and biochemically related host plants 1 , but the genetic and molecular bases for adaptation to plant defense compounds remain poorly understood 2 . We report the first whole-genome sequence of a basal lepidopteran species, Plutella xylostella, which contains 18,071 protein-coding and 1,412 unique genes with an expansion of gene families associated with perception and the detoxification of plant defense compounds. A recent expansion of retrotransposons near detoxification-related genes and a wider system used in the metabolism of plant defense compounds are shown to also be involved in the development of insecticide resistance. This work shows the genetic and molecular bases for the evolutionary success of this worldwide herbivore and offers wider insights into insect adaptation to plant feeding, as well as opening avenues for more sustainable pest management.The global pest P. xylostella (Lepidoptera: Yponomeutidae) is thought to have coevolved with the crucifer plant family 3 ( Supplementary Fig. 1) and has become the most destructive pest of economically important food crops, including rapeseed, cauliflower and cabbage 4 . Recently, the total cost of damage and management worldwide was estimated at $4-5 billion per annum 5,6 . This insect is the first species to have evolved resistance to dichlorodiphenyltrichloroethane (DDT) in the 1950s 7 and to Bacillus thuringiensis (Bt) toxins in the 1990s 8 and has developed resistance to all classes of insecticide, making it increasingly difficult to control 9,10 . P. xylostella provides an exceptional system for understanding the genetic and molecular bases of how insect herbivores cope with the broad range of plant defenses and chemicals encountered in the environment (Supplementary Fig. 2).We used a P. xylostella strain (Fuzhou-S) collected from a field in Fuzhou in southeastern China (26.08 °N, 119.28 °E) for sequencing ( Supplementary Fig. 1). Whole-genome shotgun-based Illumina sequencing of single individuals (Supplementary Table 1), even after ten generations of laboratory inbreeding, resulted in a poor initial assembly (N50 = 2.4 kb, representing the size above which 50% of the total length of the sequences is included), owing to high levels of heterozygosity ( Supplementary Figs. 3 and 4 and Supplementary Table 2). Subsequently, we sequenced 100,800 fosmid clones (comprising ~10× the genome length) to a depth of 200× ( Supplementary Fig. 5 and Supplementary Tables 3-5), assembling the resulting sequence data into 1,819 scaffolds, with an N50 of 737 kb, spanning ~394 Mb of the genome sequence (version 1; Supplementary Fig. 6 and Supplementary Table 6). The assembly covered 85.5% of a set of protein-coding ESTs (Supplementary Tables 7 and 8) generated by transcriptome sequencing 11 . Alignment of a subject scaffold against a 126-kb BAC (GenBank GU058050) from an altern...

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

“…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).…”

Agricultural production: assessment of the potential use of Cas9-mediated gene drive systems for agricultural pest control

“…DBM is prone to develop insecticide resistance, and most existing active ingredients are no longer useful against this pest (Grzywacz et al 2010). In many cases, the genetic basis of resistance to these active ingredients has been determined (You et al 2013). For some of these, it may be possible to deploy a gene-drive approach to return the resistance allele frequency to a level that would allow for management of resistance using other strategies.…”

“…For these species, a population suppression strategy is more feasible. While RNAi-based gene downregulation, through ingestion or injection, has proven highly effective in several species of Hemipterans, including Acyrthosiphon pisum, Lygus lineolaris, Oncopeltus fasciatus, Rhodnius prolixus, N. lugens, and B. tabaci (You et al 2013), more sophisticated genetic manipulations involving both gene knockout and transgenic technologies are needed for the types of genetic experiments required to validate putative virus-receptor proteins in these insects.…”

Selecting and validating reference genes for quantitative real-time PCR in Plutella xylostella (L.)

“…capitata) field in Fuzhou (26.08°N, 119.28°E) in 2004 and was subsequently reared in the laboratory under constant conditions with no exposure to insecticide (You et al 2013). Two insecticide-resistant strains (chlorpyrifos-and fipronil-resistant strains, CRS and FRS)…”

“…Historic reliance on insecticides has led to the rapid development of insecticide resistance in P. xylostella populations (Georghiou 1990), making it difficult to control. In recent years, several publications on and large databases of the species genome and transcriptome (He et al 2012;Tang et al 2014;You et al 2013) have been produced, and there has been an increasing focus on P.…”