Tissue-specific gene expression shows a cynipid wasp repurposes oak host gene networks to create a complex and novel parasite-specific organ

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 co-opt the genome machinery of its partner to expand its available tools. Insect-induced plant galls are an extreme example of this, wherein an insect hijacks the plant's genome to direct the initiation and development of galls consisting of plant tissue. However, previous transcriptomic studies have not evaluated individual tissues within a gall to determine the full extent to which a galling insect manipulates its host plant. Here we demonstrate that the cynipid wasp Dryocosmus quercuspalustris creates a complex 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 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 shows increases in various plant defence 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 for the wasp's control on gall growth.