Tissue-specific gene expression shows cynipid wasps repurpose host gene
networks to create complex and novel parasite-specific organs on oaks
Abstract
Every organism on Earth depends on interactions with other organisms to
survive. In each of these interactions, an organism must utilize the
limited toolbox of genes and proteins it possesses to successfully
manipulate or cooperate with another species, but it can also coopt the
genome machinery of its partner. Insect-induced plant galls are an
extreme example of this, wherein an insect hijacks the plant genome to
direct the initiation and development of galls comprising of plant
tissue. However, the mechanism(s) behind insect-induced gall induction
and development remain elusive. Here we demonstrate that cynipid wasp
Dryocosmus quercuspalustris create a complex and novel parasite-specific
organ from red oak tissue via massive changes in host gene expression.
Our results show that the gall wasp is not merely modifying oak leaf
tissue but creating a novel organ, resulting in extensive changes in
gene expression between galled and ungalled tissue (differential
expression in 28% of genes) and distinct gall tissue types (20% of
genes). The outer gall tissue showed increases in various plant defense
systems, which is consistent with its predicted functional role of
protecting the wasp larva. The inner larval capsule shows suppression of
large parts of the plant innate immune system and evidence for the wasp
utilizing the plant’s RNA interference mechanisms, which may be a
potential mechanism of gall induction. We also find significant overlap
between cynipid galls and agricultural gall pests, suggesting possible
shared mechanisms for this complex species interaction even in disparate
plants and insect galling guilds.