An Immunity-Triggering Effector from the Barley Smut Fungus Ustilago hordei Resides in an Ustilaginaceae-Specific Cluster Bearing Signs of Transposable Element-Assisted Evolution

Handle URI:
http://hdl.handle.net/10754/334596
Title:
An Immunity-Triggering Effector from the Barley Smut Fungus Ustilago hordei Resides in an Ustilaginaceae-Specific Cluster Bearing Signs of Transposable Element-Assisted Evolution
Authors:
Ali, Shawkat ( 0000-0003-3282-3186 ) ; Laurie, John D.; Linning, Rob; Cervantes-Chávez, José Antonio; Gaudet, Denis; Bakkeren, Guus
Abstract:
The basidiomycete smut fungus Ustilago hordei was previously shown to comprise isolates that are avirulent on various barley host cultivars. Through genetic crosses we had revealed that a dominant avirulence locus UhAvr1 which triggers immunity in barley cultivar Hannchen harboring resistance gene Ruh1, resided within an 80-kb region. DNA sequence analysis of this genetically delimited region uncovered the presence of 7 candidate secreted effector proteins. Sequence comparison of their coding sequences among virulent and avirulent parental and field isolates could not distinguish UhAvr1 candidates. Systematic deletion and complementation analyses revealed that UhAvr1 is UHOR_10022 which codes for a small effector protein of 171 amino acids with a predicted 19 amino acid signal peptide. Virulence in the parental isolate is caused by the insertion of a fragment of 5.5 kb with similarity to a common U. hordei transposable element (TE), interrupting the promoter of UhAvr1 and thereby changing expression and hence recognition of UhAVR1p. This rearrangement is likely caused by activities of TEs and variation is seen among isolates. Using GFP-chimeric constructs we show that UhAvr1 is induced only in mated dikaryotic hyphae upon sensing and infecting barley coleoptile cells. When infecting Hannchen, UhAVR1p causes local callose deposition and the production of reactive oxygen species and necrosis indicative of the immune response. UhAvr1 does not contribute significantly to overall virulence. UhAvr1 is located in a cluster of ten effectors with several paralogs and over 50% of TEs. This cluster is syntenous with clusters in closely-related U. maydis and Sporisorium reilianum. In these corn-infecting species, these clusters harbor however more and further diversified homologous effector families but very few TEs. This increased variability may have resulted from past selection pressure by resistance genes since U. maydis is not known to trigger immunity in its corn host. © 2014 Ali et al.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Center for Desert Agriculture
Citation:
Ali S, Laurie JD, Linning R, Cervantes-Chávez JA, Gaudet D, et al. (2014) An Immunity-Triggering Effector from the Barley Smut Fungus Ustilago hordei Resides in an Ustilaginaceae-Specific Cluster Bearing Signs of Transposable Element-Assisted Evolution. PLoS Pathog 10: e1004223. doi:10.1371/journal.ppat.1004223.
Publisher:
Public Library of Science (PLoS)
Journal:
PLoS Pathogens
Issue Date:
3-Jul-2014
DOI:
10.1371/journal.ppat.1004223
PubMed ID:
24992661
PubMed Central ID:
PMC4081816
Type:
Article
ISSN:
15537366
Appears in Collections:
Articles; Center for Desert Agriculture; Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorAli, Shawkaten
dc.contributor.authorLaurie, John D.en
dc.contributor.authorLinning, Roben
dc.contributor.authorCervantes-Chávez, José Antonioen
dc.contributor.authorGaudet, Denisen
dc.contributor.authorBakkeren, Guusen
dc.date.accessioned2014-11-11T14:31:24Z-
dc.date.available2014-11-11T14:31:24Z-
dc.date.issued2014-07-03en
dc.identifier.citationAli S, Laurie JD, Linning R, Cervantes-Chávez JA, Gaudet D, et al. (2014) An Immunity-Triggering Effector from the Barley Smut Fungus Ustilago hordei Resides in an Ustilaginaceae-Specific Cluster Bearing Signs of Transposable Element-Assisted Evolution. PLoS Pathog 10: e1004223. doi:10.1371/journal.ppat.1004223.en
dc.identifier.issn15537366en
dc.identifier.pmid24992661en
dc.identifier.doi10.1371/journal.ppat.1004223en
dc.identifier.urihttp://hdl.handle.net/10754/334596en
dc.description.abstractThe basidiomycete smut fungus Ustilago hordei was previously shown to comprise isolates that are avirulent on various barley host cultivars. Through genetic crosses we had revealed that a dominant avirulence locus UhAvr1 which triggers immunity in barley cultivar Hannchen harboring resistance gene Ruh1, resided within an 80-kb region. DNA sequence analysis of this genetically delimited region uncovered the presence of 7 candidate secreted effector proteins. Sequence comparison of their coding sequences among virulent and avirulent parental and field isolates could not distinguish UhAvr1 candidates. Systematic deletion and complementation analyses revealed that UhAvr1 is UHOR_10022 which codes for a small effector protein of 171 amino acids with a predicted 19 amino acid signal peptide. Virulence in the parental isolate is caused by the insertion of a fragment of 5.5 kb with similarity to a common U. hordei transposable element (TE), interrupting the promoter of UhAvr1 and thereby changing expression and hence recognition of UhAVR1p. This rearrangement is likely caused by activities of TEs and variation is seen among isolates. Using GFP-chimeric constructs we show that UhAvr1 is induced only in mated dikaryotic hyphae upon sensing and infecting barley coleoptile cells. When infecting Hannchen, UhAVR1p causes local callose deposition and the production of reactive oxygen species and necrosis indicative of the immune response. UhAvr1 does not contribute significantly to overall virulence. UhAvr1 is located in a cluster of ten effectors with several paralogs and over 50% of TEs. This cluster is syntenous with clusters in closely-related U. maydis and Sporisorium reilianum. In these corn-infecting species, these clusters harbor however more and further diversified homologous effector families but very few TEs. This increased variability may have resulted from past selection pressure by resistance genes since U. maydis is not known to trigger immunity in its corn host. © 2014 Ali et al.en
dc.language.isoenen
dc.publisherPublic Library of Science (PLoS)en
dc.rightsThis 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.en
dc.rightsArchived with thanks to PLoS Pathogensen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titleAn Immunity-Triggering Effector from the Barley Smut Fungus Ustilago hordei Resides in an Ustilaginaceae-Specific Cluster Bearing Signs of Transposable Element-Assisted Evolutionen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentCenter for Desert Agricultureen
dc.identifier.journalPLoS Pathogensen
dc.identifier.pmcidPMC4081816en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionAgriculture and Agri-Food Canada, Pacific Agri-Food Research Centre, Summerland, BC, Canadaen
dc.contributor.institutionDepartment of Botany, University of British Columbia, Vancouver, BC, Canadaen
dc.contributor.institutionAgriculture and Agri-Food Canada, Lethbridge Research Centre, Lethbridge, AB, Canadaen
dc.contributor.institutionUniversity of Nebraska-Lincoln, Center for Plant Science Innovation, Lincoln, NE, United Statesen
dc.contributor.institutionUnidad de Microbiologa Bsica y Aplicada, Campus Aeropuerto, Universidad Autnoma de Quer taro, Quer taro, Mexicoen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorAli, Shawkaten

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