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Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp

Authors: Jack Hearn; Mark Blaxter; Karsten Schönrogge; José-Luis Nieves-Aldrey; Juli Pujade-Villar; Elisabeth Huguet; Jean-Michel Drezen; +2 Authors

Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp

Abstract

Galls are plant tissues whose development is induced by another organism for the inducer's benefit. 30,000 arthropod species induce galls, and in most cases the inducing effectors and target plant systems are unknown. Cynipid gall wasps are a speciose monophyletic radiation that induce structurally complex galls on oaks and other plants. We used a model system comprising the gall wasp Biorhiza pallida and the oak Quercus robur to characterise inducer and host plant gene expression at defined stages through the development of galled and ungalled plant tissues, and tested alternative hypotheses for the origin and type of galling effectors and plant metabolic pathways involved. Oak gene expression patterns diverged markedly during development of galled and normal buds. Young galls showed elevated expression of oak genes similar to legume root nodule Nod factor-induced early nodulin (ENOD) genes and developmental parallels with oak buds. In contrast, mature galls showed substantially different patterns of gene expression to mature leaves. While most oak transcripts could be functionally annotated, many gall wasp transcripts of interest were novel. We found no evidence in the gall wasp for involvement of third-party symbionts in gall induction, for effector delivery using virus-like-particles, or for gallwasp expression of genes coding for plant hormones. Many differentially and highly expressed genes in young larvae encoded secretory peptides, which we hypothesise are effector proteins exported to plant tissues. Specifically, we propose that host arabinogalactan proteins and gall wasp chitinases interact in young galls to generate a somatic embryogenesis-like process in oak tissues surrounding the gall wasp larvae. Gall wasp larvae also expressed genes encoding multiple plant cell wall degrading enzymes (PCWDEs). These have functional orthologues in other gall inducing cynipids but not in figitid parasitoid sister groups, suggesting that they may be evolutionary innovations associated with cynipid gall induction.

Countries
France, Spain, United Kingdom
Keywords

gall-formation, Larves, Wasps, qu_475, [SDV.GEN] Life Sciences [q-bio]/Genetics, QH426-470, Host-Parasite Interactions, transcriptomics, Quercus, Larvae, Plant Growth Regulators, Gene Expression Regulation, Plant, Cynipidae, Plant Tumors, Genetics, qx_500, Animals, nod-factor, qu_500, Genomics, Expressió gènica, [SDV] Life Sciences [q-bio], arabinogalactan, Insectes, Insects, Plant Leaves, Phenotype, chitinase, Larva, Gene expression, Metabolic Networks and Pathways, Research Article

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selected citations
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This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
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popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
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