Chromosome-level genome of black cutworm provides novel insights into polyphagy and seasonal migration in insects

Abstract

Background The black cutworm, Agrotis ipsilon, is a serious global underground pest. Its distinct phenotypic traits, especially its polyphagy and ability to migrate long distances, contribute to its widening distribution and increasing difficulty of control. However, knowledge about these traits is still limited. Results We generated a high-quality chromosome-level assembly of A. ipsilon using PacBio and Hi-C technology with a contig N50 length of ~ 6.7 Mb. Comparative genomic and transcriptomic analyses showed that detoxification-associated gene families were highly expanded and induced after insects fed on specific host plants. Knockout of genes that encoded two induced ABC transporters using CRISPR/Cas9 significantly reduced larval growth rate, consistent with their contribution to host adaptation. A comparative transcriptomic analysis between tethered-flight moths and migrating moths showed expression changes in the circadian rhythm gene AiCry2 involved in sensing photoperiod variations and may receipt magnetic fields accompanied by MagR and in genes that regulate the juvenile hormone pathway and energy metabolism, all involved in migration processes. Conclusions This study provides valuable genomic resources for elucidating the mechanisms involved in moth migration and developing innovative control strategies.

Biological Characteristics and Energy Metabolism of Migrating Insects

“…For migratory insects, JH plays a key role in the regulation of migration due to the interaction between flight and reproduction [ 83 , 84 ]. The topical treatment of migratory insects with JH analogs can allow us to observe changes in their flight and reproductive activities and analyze specific regulatory effects.…”

“…Most insects, including Diptera, Hymenoptera, and some Lepidoptera, mainly use carbohydrates to provide energy for short-distance flight. Many long-distance migratory insects, including L. migratoria [ 108 ], M. sanguinipes [ 109 ], A. ipsilon [ 84 , 110 ], D. plexippus [ 111 ], M. separata [ 112 ], S. exigua [ 113 ], S. litura [ 114 ], and S. exempta [ 115 ], are generally powered by carbohydrates at the initial stage of flight activities; then, they mainly use the lipid substances stored in the fat body as the energy supply for continuous long-distance flight [ 10 , 116 , 117 , 118 ]. Some insects, such as the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) [ 119 , 120 ], and some bees and wasps [ 121 , 122 ], can also use proline oxidative metabolism to supply energy for flight.…”

“…Omics studies have shown that genetic information related to energy metabolism, the interaction between migration and reproduction, hormone synthesis, etc. is the molecular basis for the long-distance migration of insects [ 83 , 84 , 191 , 192 , 193 ]. However, the key environmental factors that induce insect migration are still unclear.…”

Epsilon Class Glutathione S-Transferase Confers Phoxim Tolerance in the Black Cutworm Agrotis ipsilon (Lepidoptera: Noctuidae)

“…The cDNA sequences of AiGSTe1 were identified by retrieving the A. ipsilon transcriptome data set 19 using the TBLASTN algorithm in the Basic Local Alignment Search Tool (BLAST). The amino acid sequence of S. litura SlGSTe1 (GenBank accession number: AY506545) was used as the query, and the expected value (e-value) was set as 1 × 10 −5 .…”

“…19 Annotation of the genome reveals at least 42 GST genes and the epsilon class GSTs are remarkably expanded in the genome. 19 The widespread expansion of epsilon class GSTs might be involved in the metabolism of phoxim and enhance the tolerance of A. ipsilon to the insecticide. However, to date, research on epsilon class GSTs and their detoxification functions in A. ipsilon has been limited.…”