WRR4 Encodes a TIR-NB-LRR Protein That Confers Broad-Spectrum White Rust Resistance in Arabidopsis thaliana to Four Physiological Races of Albugo candida

White blister rust in the Brassicaceae is emerging as a superb model for exploring how plant biodiversity has channeled speciation of biotrophic parasites. The causal agents of white rust across a wide breadth of cruciferous hosts currently are named as variants of a single oomycete species, Albugo...

Full description

Bibliographic Details
Main Authors: M. Hossein Borhan, Nick Gunn, Abigail Cooper, Sigrun Gulden, Mahmut Tör, S. Roger Rimmer, Eric B. Holub
Format: Article
Language:English
Published: The American Phytopathological Society 2008-06-01
Series:Molecular Plant-Microbe Interactions
Subjects:
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-21-6-0757
_version_ 1818647188091174912
author M. Hossein Borhan
Nick Gunn
Abigail Cooper
Sigrun Gulden
Mahmut Tör
S. Roger Rimmer
Eric B. Holub
author_facet M. Hossein Borhan
Nick Gunn
Abigail Cooper
Sigrun Gulden
Mahmut Tör
S. Roger Rimmer
Eric B. Holub
author_sort M. Hossein Borhan
collection DOAJ
description White blister rust in the Brassicaceae is emerging as a superb model for exploring how plant biodiversity has channeled speciation of biotrophic parasites. The causal agents of white rust across a wide breadth of cruciferous hosts currently are named as variants of a single oomycete species, Albugo candida. The most notable examples include a major group of physiological races that each are economically destructive in a different vegetable or oilseed crop of Brassica juncea (A. candida race 2), B. rapa (race 7), or B. oleracea (race 9); or parasitic on wild crucifers such as Capsella bursa-pastoris (race 4). Arabidopsis thaliana is innately immune to these races of A. candida under natural conditions; however, it commonly hosts its own molecularly distinct subspecies of A. candida (A. candida subsp. arabidopsis). In the laboratory, we have identified several accessions of Arabidopsis thaliana (e.g.,. Ws-3) that can permit varying degrees of rust development following inoculation with A. candida races 2, 4, and 7, whereas race 9 is universally incompatible in Arabidopsis thaliana and nonrusting resistance is the most prevalent outcome of interactions with the other races. Subtle variation in resistance phenotypes is evident, observed initially with an isolate of A. candida race 4, indicating additional genetic variation. Therefore, we used the race 4 isolate for map-based cloning of the first of many expected white rust resistance (WRR) genes. This gene was designated WRR4 and encodes a cytoplasmic toll-interleukin receptor-like nucleotide-binding leucine-rich repeat receptor-like protein that confers a dominant, broad-spectrum white rust resistance in the Arabidopsis thaliana accession Columbia to representative isolates of A. candida races 2, 4, 7, and 9, as verified by transgenic expression of the Columbia allele in Ws-3. The WRR4 protein requires functional expression of the lipase-like protein EDS1 but not the paralogous protein PAD4, and confers full immunity that masks an underlying nonhypersensitive incompatibility in Columbia to A. candida race 4. This residual incompatibility is independent of functional EDS1.
first_indexed 2024-12-17T00:58:33Z
format Article
id doaj.art-dfdf04afdf68440496cc405d3abcb8b8
institution Directory Open Access Journal
issn 0894-0282
1943-7706
language English
last_indexed 2024-12-17T00:58:33Z
publishDate 2008-06-01
publisher The American Phytopathological Society
record_format Article
series Molecular Plant-Microbe Interactions
spelling doaj.art-dfdf04afdf68440496cc405d3abcb8b82022-12-21T22:09:32ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062008-06-0121675776810.1094/MPMI-21-6-0757WRR4 Encodes a TIR-NB-LRR Protein That Confers Broad-Spectrum White Rust Resistance in Arabidopsis thaliana to Four Physiological Races of Albugo candidaM. Hossein BorhanNick GunnAbigail CooperSigrun GuldenMahmut TörS. Roger RimmerEric B. HolubWhite blister rust in the Brassicaceae is emerging as a superb model for exploring how plant biodiversity has channeled speciation of biotrophic parasites. The causal agents of white rust across a wide breadth of cruciferous hosts currently are named as variants of a single oomycete species, Albugo candida. The most notable examples include a major group of physiological races that each are economically destructive in a different vegetable or oilseed crop of Brassica juncea (A. candida race 2), B. rapa (race 7), or B. oleracea (race 9); or parasitic on wild crucifers such as Capsella bursa-pastoris (race 4). Arabidopsis thaliana is innately immune to these races of A. candida under natural conditions; however, it commonly hosts its own molecularly distinct subspecies of A. candida (A. candida subsp. arabidopsis). In the laboratory, we have identified several accessions of Arabidopsis thaliana (e.g.,. Ws-3) that can permit varying degrees of rust development following inoculation with A. candida races 2, 4, and 7, whereas race 9 is universally incompatible in Arabidopsis thaliana and nonrusting resistance is the most prevalent outcome of interactions with the other races. Subtle variation in resistance phenotypes is evident, observed initially with an isolate of A. candida race 4, indicating additional genetic variation. Therefore, we used the race 4 isolate for map-based cloning of the first of many expected white rust resistance (WRR) genes. This gene was designated WRR4 and encodes a cytoplasmic toll-interleukin receptor-like nucleotide-binding leucine-rich repeat receptor-like protein that confers a dominant, broad-spectrum white rust resistance in the Arabidopsis thaliana accession Columbia to representative isolates of A. candida races 2, 4, 7, and 9, as verified by transgenic expression of the Columbia allele in Ws-3. The WRR4 protein requires functional expression of the lipase-like protein EDS1 but not the paralogous protein PAD4, and confers full immunity that masks an underlying nonhypersensitive incompatibility in Columbia to A. candida race 4. This residual incompatibility is independent of functional EDS1.https://apsjournals.apsnet.org/doi/10.1094/MPMI-21-6-0757basidiomycetegene-for-geneinnate immunityLeptosphaerianatural variationnonhost
spellingShingle M. Hossein Borhan
Nick Gunn
Abigail Cooper
Sigrun Gulden
Mahmut Tör
S. Roger Rimmer
Eric B. Holub
WRR4 Encodes a TIR-NB-LRR Protein That Confers Broad-Spectrum White Rust Resistance in Arabidopsis thaliana to Four Physiological Races of Albugo candida
Molecular Plant-Microbe Interactions
basidiomycete
gene-for-gene
innate immunity
Leptosphaeria
natural variation
nonhost
title WRR4 Encodes a TIR-NB-LRR Protein That Confers Broad-Spectrum White Rust Resistance in Arabidopsis thaliana to Four Physiological Races of Albugo candida
title_full WRR4 Encodes a TIR-NB-LRR Protein That Confers Broad-Spectrum White Rust Resistance in Arabidopsis thaliana to Four Physiological Races of Albugo candida
title_fullStr WRR4 Encodes a TIR-NB-LRR Protein That Confers Broad-Spectrum White Rust Resistance in Arabidopsis thaliana to Four Physiological Races of Albugo candida
title_full_unstemmed WRR4 Encodes a TIR-NB-LRR Protein That Confers Broad-Spectrum White Rust Resistance in Arabidopsis thaliana to Four Physiological Races of Albugo candida
title_short WRR4 Encodes a TIR-NB-LRR Protein That Confers Broad-Spectrum White Rust Resistance in Arabidopsis thaliana to Four Physiological Races of Albugo candida
title_sort wrr4 encodes a tir nb lrr protein that confers broad spectrum white rust resistance in arabidopsis thaliana to four physiological races of albugo candida
topic basidiomycete
gene-for-gene
innate immunity
Leptosphaeria
natural variation
nonhost
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-21-6-0757
work_keys_str_mv AT mhosseinborhan wrr4encodesatirnblrrproteinthatconfersbroadspectrumwhiterustresistanceinarabidopsisthalianatofourphysiologicalracesofalbugocandida
AT nickgunn wrr4encodesatirnblrrproteinthatconfersbroadspectrumwhiterustresistanceinarabidopsisthalianatofourphysiologicalracesofalbugocandida
AT abigailcooper wrr4encodesatirnblrrproteinthatconfersbroadspectrumwhiterustresistanceinarabidopsisthalianatofourphysiologicalracesofalbugocandida
AT sigrungulden wrr4encodesatirnblrrproteinthatconfersbroadspectrumwhiterustresistanceinarabidopsisthalianatofourphysiologicalracesofalbugocandida
AT mahmuttor wrr4encodesatirnblrrproteinthatconfersbroadspectrumwhiterustresistanceinarabidopsisthalianatofourphysiologicalracesofalbugocandida
AT srogerrimmer wrr4encodesatirnblrrproteinthatconfersbroadspectrumwhiterustresistanceinarabidopsisthalianatofourphysiologicalracesofalbugocandida
AT ericbholub wrr4encodesatirnblrrproteinthatconfersbroadspectrumwhiterustresistanceinarabidopsisthalianatofourphysiologicalracesofalbugocandida