Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation

TLDR

The brown planthopper is the most destructive rice pest, a monophagous sap‑sucking insect that outbreaks every three years in Asia and serves as a model for ecological studies and pest‑management research. To elucidate how this herbivore has adapted to exclusive rice feeding and to inform control strategies, the authors sequenced the brown planthopper genome and its two endosymbionts. They present a 1.14‑gigabase draft genome of the planthopper and the genomes of two microbial endosymbionts that enable the insect to thrive on rice sap. The genome reveals extensive gene loss—only 40.8% of protein‑coding genes are shared with other arthropods—and shows that missing genes in essential biochemical pathways are supplied by endosymbionts, highlighting complex adaptations that support exclusive rice host use and pointing to potential pest‑control targets.

Abstract

The brown planthopper, Nilaparvata lugens, the most destructive pest of rice, is a typical monophagous herbivore that feeds exclusively on rice sap, which migrates over long distances. Outbreaks of it have re-occurred approximately every three years in Asia. It has also been used as a model system for ecological studies and for developing effective pest management. To better understand how a monophagous sap-sucking arthropod herbivore has adapted to its exclusive host selection and to provide insights to improve pest control, we analyzed the genomes of the brown planthopper and its two endosymbionts. We describe the 1.14 gigabase planthopper draft genome and the genomes of two microbial endosymbionts that permit the planthopper to forage exclusively on rice fields. Only 40.8% of the 27,571 identified Nilaparvata protein coding genes have detectable shared homology with the proteomes of the other 14 arthropods included in this study, reflecting large-scale gene losses including in evolutionarily conserved gene families and biochemical pathways. These unique genomic features are functionally associated with the animal's exclusive plant host selection. Genes missing from the insect in conserved biochemical pathways that are essential for its survival on the nutritionally imbalanced sap diet are present in the genomes of its microbial endosymbionts, which have evolved to complement the mutualistic nutritional needs of the host. Our study reveals a series of complex adaptations of the brown planthopper involving a variety of biological processes, that result in its highly destructive impact on the exclusive host rice. All these findings highlight potential directions for effective pest control of the planthopper.