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Tissue-specific gene expression shows cynipid wasps repurpose host gene networks to create complex and novel parasite-specific organs on oaks
  • Ellen Martinson,
  • John Werren,
  • Scott Egan
Ellen Martinson
University of New Mexico
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John Werren
University of Rochester
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Scott Egan
Rice University
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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.

Peer review status:Published

12 Sep 2021Published in Molecular Ecology. 10.1111/mec.16159