How 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 plants¹, but the genetic and molecular bases for adaptation to plant defense compounds remain poorly understood². 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.

Tea is an important global beverage crop and is largely clonally propagated. Despite previous studies on the species, its genetic and evolutionary history deserves further research. Here, we present a haplotype-resolved assembly of an Oolong tea cultivar, Tieguanyin. Analysis of allele-specific expression suggests a potential mechanism in response to mutation load during long-term clonal propagation. Population genomic analysis using 190 Camellia accessions uncovered independent evolutionary histories and parallel domestication in two widely cultivated varieties, var. sinensis and var. assamica. It also revealed extensive intra- and interspecific introgressions contributing to genetic diversity in modern cultivars. Strong signatures of selection were associated with biosynthetic and metabolic pathways that contribute to flavor characteristics as well as genes likely involved in the Green Revolution in the tea industry. Our results offer genetic and molecular insights into the evolutionary history of Camellia sinensis and provide genomic resources to further facilitate gene editing to enhance desirable traits in tea crops.

The diamondback moth (DBM), Plutella xylostella (L.), costs the Chinese economy US$0.77 billion annually, and considerable research has focused on its biology, ecology, and management. Much of this research has been published locally and is inaccessible outside China. Since 1990 Brassica vegetable production has increased 20-fold and production practices have intensified, but losses continue to increase. Insecticide use is widespread and many DBM populations, particularly in southern provinces, are resistant to multiple compounds. The molecular bases of several insecticide resistance mechanisms are well understood, and genetic studies suggest that insecticide-resistant populations migrate northward in spring and that back migrations may occur in southern provinces. Fundamental studies have improved our understanding of the effects of temperature on DBM population dynamics and distributions and of interactions between DBM and its well-established parasitoid fauna. Nationally coordinated research is developing regional management strategies that integrate locally appropriate biological, physical, cultural, and insecticidal control, but sustaining their adoption will prove an enormous challenge.

The development of insecticide resistance in insect pests is a worldwide concern and elucidating the underlying mechanisms is critical for effective crop protection. Recent studies have indicated potential links between insect gut microbiota and insecticide resistance and these may apply to the diamondback moth, Plutella xylostella (L.), a globally and economically important pest of cruciferous crops. We isolated Enterococcus sp. (Firmicutes), Enterobacter sp. (Proteobacteria), and Serratia sp. (Proteobacteria) from the guts of P. xylostella and analyzed the effects on, and underlying mechanisms of insecticide resistance. Enterococcus sp. enhanced resistance to the widely used insecticide, chlorpyrifos, in P. xylostella, while in contrast, Serratia sp. decreased resistance and Enterobacter sp. and all strains of heat-killed bacteria had no effect. Importantly, the direct degradation of chlorpyrifos in vitro was consistent among the three strains of bacteria. We found that Enterococcus sp., vitamin C, and acetylsalicylic acid enhanced insecticide resistance in P. xylostella and had similar effects on expression of P. xylostella antimicrobial peptides. Expression of cecropin was down-regulated by the two compounds, while gloverin was up-regulated. Bacteria that were not associated with insecticide resistance induced contrasting gene expression profiles to Enterococcus sp. and the compounds. Our studies confirmed that gut bacteria play an important role in P. xylostella insecticide resistance, but the main mechanism is not direct detoxification of insecticides by gut bacteria. We also suggest that the influence of gut bacteria on insecticide resistance may depend on effects on the immune system. Our work advances understanding of the evolution of insecticide resistance in this key pest and highlights directions for research into insecticide resistance in other insect pest species.

Insect midgut microbiota is important in host nutrition, development and immune response. Recent studies indicate possible links between insect gut microbiota and resistance to biological and chemical toxins. Studies of this phenomenon and symbionts in general have been hampered by difficulties in culture-based approach. In the present study, DNA sequencing was used to examine the midgut microbiota of diamondback moth (DBM), Plutella xylostella (L.), a destructive pest that attacks cruciferous crops worldwide. Its ability to develop resistance to many types of synthetic insecticide and even Bacillus thuringiensis toxins makes it an important species to study. Bacteria of the DBM larval midgut in a susceptible and two insecticide (chlorpyrifos and fipronil) resistant lines were examined by Illumina sequencing sampled from an insect generation that was not exposed to insecticide. This revealed that more than 97% of the bacteria were from three orders: Enterobacteriales, Vibrionales and Lactobacillales. Both insecticide-resistant lines had more Lactobacillales and the much scarcer taxa Pseudomonadales and Xanthomonadales with fewer Enterobacteriales compared with the susceptible strain. Consistent with this, a second study observed an increase in the proportion of Lactobacillales in the midgut of DBM individuals from a generation treated with insecticides. This is the first report of high-throughput DNA sequencing of the entire microbiota of DBM. It reveals differences related to inter- and intra-generational exposure to insecticides. Differences in the midgut microbiota among susceptible and insecticide-resistant lines are independent of insecticide exposure in the sampled generations. While this is consistent with the hypothesis that Lactobacillales or other scarcer taxa play a role in conferring DBM insecticide resistance, further studies are necessary to rule out other possibilities. Findings constitute the basis for future molecular work on the functions of insect midgut microbiota taxa and their possible role in conferring host resistance to toxins.

Herbivore specialists adapt to feed on a specific group of host plants by evolving various mechanisms to respond to plant defences. Insects also possess complex gut microbiotas but their potential role in adaptation is poorly understood. Our previous study of the genome of diamondback moth, Plutella xylostella, revealed an intrinsic capacity to detoxify plant defence compounds, which is an important factor in its success as a pest. Here we expand on that work with a complete taxonomic and functional profile of the P. xylostella gut microbiota obtained by metagenomic sequencing. Gene enrichment in the metagenome, accompanied by functional identification, revealed an important role of specific gut bacteria in the breakdown of plant cell walls, detoxification of plant phenolics, and synthesis of amino acids. Microbes participating in these pathways mainly belonged to three highly abundant bacteria: Enterobacter cloacae, Enterobacter asburiae, and Carnobacterium maltaromaticum. Results show that while the gut microbial community may be complex, a small number of functionally active species can be disproportionally important. The presence of specific enzymes in the microbiota community, such as supporting amino acid synthesis, digestion and detoxification functions, demonstrates the beneficial interactions between P. xylostella and its gut microbiota. These interactions can be potential targets for manipulation to provide novel pest management approaches.