| description |
Plant galls are dramatic examples of extended phenotypes, in which plant development is hijacked to produce novel tissues and structures that benefit another organism. The genetic processes underlying gall induction are largely unknown. A radiation of cynipid gallwasps induces some of the most dramatic and complex galls on oaks, and we studied one oak gallwasp (Biorhiza pallida) and its host oak (Quercus petraea), using transcriptome and genome sequencing, to identify parasite and host genes active through gall development. These data were used to test alternative hypotheses for gall induction and maintenance. We identified multiple oak and gallwasp genes that were differentially and highly expressed in young galls. While most of the oak transcripts could be functionally annotated, most gallwasp transcripts were novel. What are galls, in plant terms? Young gall tissues had gene expression patterns congruent with oak somatic embryogenesis, with elevated expression of loci similar to legume root nodule Nod factor-induced ENOD genes, and of biotin carboxyl carrier proteins, indicative of high fatty acid metabolism. These features are consistent with the hypothesis that galls show developmental parallels with seeds. How are galls first induced? We found no evidence for involvement of symbiotic viruses or microorganisms in gall induction, or for gallwasp utilization of virus-like particles for delivery of gall inducing stimuli. We also found no evidence for gallwasp production of plant hormone homologues. Many of the differentially and highly expressed genes in young larvae had secretory peptides, suggesting that they may be part of the induction system. Young larvae showed high expression of two chitinase enzymes, which may act on the host ENOD-like proteins to induce the somatic embryogenesis-like state. Gallwasp larvae expressed multiple plant cell wall degrading enzymes (PCWDEs), whose sequences suggested horizontal gene transfer from bacteria. Comparing genome data from related galling and non-galling wasp species, we found orthologues of B. pallida PCWDEs only in the most closely related non-galling relatives. Cynipid galls on oaks thus are structures with both seed- and somatic embryo-like features, specifically induced by gall wasp nuclear genes that include a range of horizontally acquired effectors also active in other instances of the pathogen-plant interface. |