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

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 structur...

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Autores principales: Hearn, Jack, Blaxter, Mark, Schönrogge, Karsten, Nieves-Aldrey, José-Luis, Pujade-Villar, Juli, Huguet, Elisabeth, Drezen, Jean-Michel, Shorthouse, Joseph D., Stone, Graham N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6855507/
https://www.ncbi.nlm.nih.gov/pubmed/31682601
http://dx.doi.org/10.1371/journal.pgen.1008398
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author Hearn, Jack
Blaxter, Mark
Schönrogge, Karsten
Nieves-Aldrey, José-Luis
Pujade-Villar, Juli
Huguet, Elisabeth
Drezen, Jean-Michel
Shorthouse, Joseph D.
Stone, Graham N.
author_facet Hearn, Jack
Blaxter, Mark
Schönrogge, Karsten
Nieves-Aldrey, José-Luis
Pujade-Villar, Juli
Huguet, Elisabeth
Drezen, Jean-Michel
Shorthouse, Joseph D.
Stone, Graham N.
author_sort Hearn, Jack
collection PubMed
description 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.
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spelling pubmed-68555072019-12-06 Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp Hearn, Jack Blaxter, Mark Schönrogge, Karsten Nieves-Aldrey, José-Luis Pujade-Villar, Juli Huguet, Elisabeth Drezen, Jean-Michel Shorthouse, Joseph D. Stone, Graham N. PLoS Genet Research Article 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. Public Library of Science 2019-11-04 /pmc/articles/PMC6855507/ /pubmed/31682601 http://dx.doi.org/10.1371/journal.pgen.1008398 Text en © 2019 Hearn et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Hearn, Jack
Blaxter, Mark
Schönrogge, Karsten
Nieves-Aldrey, José-Luis
Pujade-Villar, Juli
Huguet, Elisabeth
Drezen, Jean-Michel
Shorthouse, Joseph D.
Stone, Graham N.
Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp
title Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp
title_full Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp
title_fullStr Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp
title_full_unstemmed Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp
title_short Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp
title_sort genomic dissection of an extended phenotype: oak galling by a cynipid gall wasp
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6855507/
https://www.ncbi.nlm.nih.gov/pubmed/31682601
http://dx.doi.org/10.1371/journal.pgen.1008398
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