Abstract

Locusts exhibit remarkable density-dependent phenotype (phase) changes from the solitary to the gregarious, making them one of the most destructive agricultural pests. This phenotype polyphenism arises from a single genome and diverse transcriptomes in different conditions. Here we report a de novo transcriptome for the migratory locust and a comprehensive, representative core gene set. We carried out assembly of 21.5 Gb Illumina reads, generated 72,977 transcripts with N50 2,275 bp and identified 11,490 locust protein-coding genes. Comparative genomics analysis with eight other sequenced insects was carried out to indentify the genomic divergence between hemimetabolous and holometabolous insects for the first time and 18 genes relevant to development was found. We further utilized the quantitative feature of RNA-seq to measure and compare gene expression among libraries. We first discovered how divergence in gene expression between two phases progresses as locusts develop and identified 242 transcripts as candidates for phase marker genes. Together with the detailed analysis of deep sequencing data of the 4th instar, we discovered a phase-dependent divergence of biological investment in the molecular level. Solitary locusts have higher activity in biosynthetic pathways while gregarious locusts show higher activity in environmental interaction, in which genes and pathways associated with regulation of neurotransmitter activities, such as neurotransmitter receptors, synthetase, transporters, and GPCR signaling pathways, are strongly involved. Our study, as the largest de novo transcriptome to date, with optimization of sequencing and assembly strategy, can further facilitate the application of de novo transcriptome. The locust transcriptome enriches genetic resources for hemimetabolous insects and our understanding of the origin of insect metamorphosis. Most importantly, we identified genes and pathways that might be involved in locust development and phase change, and may thus benefit pest management.

Highlights

  • Locusts are one of the most destructive agricultural pests in the world, causing considerable economic and ecological damage

  • Based on our 12 libraries of gregarious and solitary locusts at various developmental stages, we investigated how phase differences gradually progress as locusts develop and identified genes and pathways that can be used to interrogate the molecular and genetic bases involved in development and phase changes in the migratory locust

  • We constructed 12 cDNA libraries derived from whole bodies of gregarious and solitary migratory locusts (Locusta migratoria) in six different developmental stages: egg, combined 1st and 2nd instar, 3rd instar, 4th instar, 5th instar, and adult, and deeply sequenced two samples: the gregarious and solitary 4th instar locusts (G4 and S4), generating 376 million paired-end (PE) reads with read lengths ranging from 45 bp– 75 bp

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Summary

Introduction

Locusts are one of the most destructive agricultural pests in the world, causing considerable economic and ecological damage. When the population density reaches a critical threshold, they aggregate and enter an active, gregarious phase resulting in bands of nymph and migratory swarms of adults, both of which cause millions of dollars worth of agricultural crop losses. This phenotypic plasticity in locusts results from the interplay between the environment and gene expression, including regulation of transcription, translation, and hormonal regulation, etc

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