A novel family of secreted insect proteins linked to plant gall development

Aishwarya Korgaonkar,Clair Han,Andrew L Lemire,Igor Siwanowicz,Djawed Bennouna,Rachel E Kopec,Peter Andolfatto,Shuji Shigenobu,David L Stern

doi:10.1016/j.cub.2021.01.104

Abstract

In an elaborate form of inter-species exploitation, many insects hijack plant development to induce novel plant organs called galls that provide the insect with a source of nutrition and a temporary home. Galls result from dramatic reprogramming of plant cell biology driven by insect molecules, but the roles of specific insect molecules in gall development have not yet been determined. Here, we study the aphid Hormaphis cornu, which makes distinctive "cone" galls on leaves of witch hazel Hamamelis virginiana. We found that derived genetic variants in the aphid gene determinant of gall color (dgc) are associated with strong downregulation of dgc transcription in aphid salivary glands, upregulation in galls of seven genes involved in anthocyanin synthesis, and deposition of two red anthocyanins in galls. We hypothesize that aphids inject DGC protein into galls and that this results in differential expression of a small number of plant genes. dgc is a member of a large, diverse family of novel predicted secreted proteins characterized by a pair of widely spaced cysteine-tyrosine-cysteine (CYC) residues, which we named BICYCLE proteins. bicycle genes are most strongly expressed in the salivary glands specifically of galling aphid generations, suggesting that they may regulate many aspects of gall development. bicycle genes have experienced unusually frequent diversifying selection, consistent with their potential role controlling gall development in a molecular arms race between aphids and their host plants.

Highlights

Organisms often exploit individuals of other species, for example, through predation or parasitism
We sequenced and annotated the genome of H. cornu (Figures S1A and S1B; STAR methods) and performed a genome-wide association study (GWAS) on fundatrices isolated from 43 green galls and 47 red galls by resequencing their genomes to approximately 33 coverage
Multiple observed genotypes are consistent with recombination between these 11 SNPs (Figure 2E), and we found no evidence for chromosomal aberrations that could suppress recombination (Figures S1G–S1K; STAR methods)

Summary

Introduction

Organisms often exploit individuals of other species, for example, through predation or parasitism. In many less-well-studied systems, parasites extract nutrients from their hosts, but they alter host behavior, physiology, or development to the parasite’s advantage.[4] Insect galls represent one of the most extreme forms of such inter-species manipulation. Insect-induced galls are intricately patterned homes that provide insects with protection from environmental vicissitude and from some predators and parasites.[5,6,7] Galls are resource sinks, drawing nutrients from distant plant organs and providing insects with abundant food.[8] Insect galls are atypical plant growths that do not result from unpatterned cellular over-proliferation, as observed for microbial galls, like the crown gall induced by Agrobacterium tumefaciens. Each galling insect species appears to induce a distinctive gall, even when related insect species attack the same plant, implying that each species provides unique instructions to reprogram latent plant developmental networks.[9,10,11,12,13,14,15,16,17,18,19]

Methods

Results

Discussion

Conclusion