BackgroundThe 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.ResultsWe 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-014-0521-0) contains supplementary material, which is available to authorized users.

Upon feeding, mosquito midguts secrete the peritrophic matrix (PM), an extracellular chitin-containing envelope that completely surrounds the blood meal. Because the malaria parasite must cross the PM to complete its life cycle in the mosquito, the PM is a potential barrier for malaria transmission. By antibody screening of an expression library we have identified and partially characterized a cDNA encoding a putative PM protein, termed Anopheles gambiae adult peritrophin 1 (Ag-Aper1). Ag-Aper1 is the first cloned PM gene from a disease vector. Northern analysis detected an abundant Ag-Aper1 transcript only in the adult gut, and not in any other tissues or at any other stages of development. The predicted amino acid sequence indicates that it has two tandem chitin-binding domains that share high sequence similarity with each other and also with the chitin-binding domain of an adult gut-specific chitinase from the same organism. The presumed ability of Ag-Aper1 to bind chitin was verified by a functional assay with the baculovirus-expressed recombinant protein. Ag-Aper1 did bind to chitin but not to cellulose, indicating that Ag-Aper1 binds chitin specifically. The double chitin-binding domain organization of Ag-Aper1 suggests that each protein molecule is able to link two chitin polymer chains. Hence, this protein is likely to act as a molecular linker that connects PM chitin fibrils into a three-dimensional network.

Analysis of a group of invertebrate proteins, including chitinases and peritrophic matrix proteins, reveals the presence of chitin-binding domains that share significant amino acid sequence similarity. The data suggest that these domains evolved from a common ancestor which may be a protein containing a single chitin-binding domain. The duplication and transposition of this chitin-binding domain may have contributed to the functional diversification of chitin-binding proteins. Sequence comparisons indicated that invertebrate and plant chitin binding domains do not share significant amino acid sequence similarity, suggesting that they are not coancestral. However, both the invertebrate and the plant chitin-binding domains are cysteine-rich and have several highly conserved aromatic residues. In plants, cysteines have been elucidated in maintaining protein folding and aromatic amino acids in interacting with saccharides [Wright HT, Sanddrasegaram G, Wright CS (1991) J Mol Evol 33:283-294]. It is likely that these residues perform similar functions in invertebrates. We propose that the invertebrate and the plant chitin-binding domains share similar mechanisms for folding and saccharide binding and that they evolved by convergent evolution. Furthermore, we propose that the disulfide bonds and aromatic residues are hallmarks for saccharide-binding proteins.