Evolutionary trade-offs at the Arabidopsis WRR4A resistance locus underpin alternate Albugo candida race recognition specificities

Baptiste Castel; Sebastian Fairhead; Oliver J. Furzer; Amey Redkar; Shanshan Wang; Volkan Cevik; Eric B. Holub; Jonathan D.G. Jones

doi:10.1111/tpj.15396

Evolutionary trade-offs at the Arabidopsis WRR4A resistance locus underpin alternate Albugo candida race recognition specificities

Baptiste Castel, Sebastian Fairhead, Oliver J. Furzer, Amey Redkar, Shanshan Wang, Volkan Cevik, Eric B. Holub, Jonathan D.G. Jones

Department of Life Sciences

Research output: Contribution to journal › Article › peer-review

5 Citations (SciVal)

Abstract

The oomycete Albugo candida causes white rust of Brassicaceae, including vegetable and oilseed crops, and wild relatives such as Arabidopsis thaliana. Novel White Rust Resistance (WRR) genes from Arabidopsis enable new insights into plant/parasite co-evolution. WRR4A from Arabidopsis accession Columbia (Col-0) provides resistance to many but not all white rust races, and encodes a nucleotide-binding, leucine-rich repeat immune receptor. Col-0 WRR4A resistance is broken by AcEx1, an isolate of A. candida. We identified an allele of WRR4A in Arabidopsis accession Øystese-0 (Oy-0) and other accessions that confers full resistance to AcEx1. WRR4A^Oy-0 carries a C-terminal extension required for recognition of AcEx1, but reduces recognition of several effectors recognized by the WRR4A^Col-0 allele. WRR4A^Oy-0 confers full resistance to AcEx1 when expressed in the oilseed crop Camelina sativa.

Original language	English
Pages (from-to)	1490-1502
Number of pages	13
Journal	Plant Journal
Volume	107
Issue number	5
DOIs	https://doi.org/10.1111/tpj.15396
Publication status	Published - 30 Sept 2021

Bibliographical note

Funding Information:
We thank the Gatsby Foundation (UK) for funding to the Jones lab. We thank Mark Youles in TSL Synbio for his excellent support with Golden Gate cloning and for providing modules. This research was supported in part by the NBI Computing infrastructure for Science (CiS) group and Dan MacLean’s group by providing computational infrastructure. BC, SF, OF, and VC were supported by Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/L011646/1. AR was supported by EMBO LTF (ALTF‐842‐ 2015). BC, SW, and JDGJ were supported in part by ERC Advanced Investigator grant to JDGJ ‘ImmunityByPairDesign’ Project ID 669926.

Keywords

Arabidopsis thaliana
camelina
crop protection
effector recognition
evolution
immunity
natural variation
NLR
resistance gene

ASJC Scopus subject areas

Genetics
Plant Science
Cell Biology

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10.1111/tpj.15396Licence: CC BY

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title = "Evolutionary trade-offs at the Arabidopsis WRR4A resistance locus underpin alternate Albugo candida race recognition specificities",

abstract = "The oomycete Albugo candida causes white rust of Brassicaceae, including vegetable and oilseed crops, and wild relatives such as Arabidopsis thaliana. Novel White Rust Resistance (WRR) genes from Arabidopsis enable new insights into plant/parasite co-evolution. WRR4A from Arabidopsis accession Columbia (Col-0) provides resistance to many but not all white rust races, and encodes a nucleotide-binding, leucine-rich repeat immune receptor. Col-0 WRR4A resistance is broken by AcEx1, an isolate of A. candida. We identified an allele of WRR4A in Arabidopsis accession {\O}ystese-0 (Oy-0) and other accessions that confers full resistance to AcEx1. WRR4AOy-0 carries a C-terminal extension required for recognition of AcEx1, but reduces recognition of several effectors recognized by the WRR4ACol-0 allele. WRR4AOy-0 confers full resistance to AcEx1 when expressed in the oilseed crop Camelina sativa.",

keywords = "Arabidopsis thaliana, camelina, crop protection, effector recognition, evolution, immunity, natural variation, NLR, resistance gene",

author = "Baptiste Castel and Sebastian Fairhead and Furzer, {Oliver J.} and Amey Redkar and Shanshan Wang and Volkan Cevik and Holub, {Eric B.} and Jones, {Jonathan D.G.}",

note = "Funding Information: We thank the Gatsby Foundation (UK) for funding to the Jones lab. We thank Mark Youles in TSL Synbio for his excellent support with Golden Gate cloning and for providing modules. This research was supported in part by the NBI Computing infrastructure for Science (CiS) group and Dan MacLean{\textquoteright}s group by providing computational infrastructure. BC, SF, OF, and VC were supported by Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/L011646/1. AR was supported by EMBO LTF (ALTF‐842‐ 2015). BC, SW, and JDGJ were supported in part by ERC Advanced Investigator grant to JDGJ {\textquoteleft}ImmunityByPairDesign{\textquoteright} Project ID 669926. ",

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AU - Castel, Baptiste

AU - Fairhead, Sebastian

AU - Furzer, Oliver J.

AU - Redkar, Amey

AU - Wang, Shanshan

AU - Cevik, Volkan

AU - Holub, Eric B.

AU - Jones, Jonathan D.G.

N1 - Funding Information: We thank the Gatsby Foundation (UK) for funding to the Jones lab. We thank Mark Youles in TSL Synbio for his excellent support with Golden Gate cloning and for providing modules. This research was supported in part by the NBI Computing infrastructure for Science (CiS) group and Dan MacLean’s group by providing computational infrastructure. BC, SF, OF, and VC were supported by Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/L011646/1. AR was supported by EMBO LTF (ALTF‐842‐ 2015). BC, SW, and JDGJ were supported in part by ERC Advanced Investigator grant to JDGJ ‘ImmunityByPairDesign’ Project ID 669926.

PY - 2021/9/30

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N2 - The oomycete Albugo candida causes white rust of Brassicaceae, including vegetable and oilseed crops, and wild relatives such as Arabidopsis thaliana. Novel White Rust Resistance (WRR) genes from Arabidopsis enable new insights into plant/parasite co-evolution. WRR4A from Arabidopsis accession Columbia (Col-0) provides resistance to many but not all white rust races, and encodes a nucleotide-binding, leucine-rich repeat immune receptor. Col-0 WRR4A resistance is broken by AcEx1, an isolate of A. candida. We identified an allele of WRR4A in Arabidopsis accession Øystese-0 (Oy-0) and other accessions that confers full resistance to AcEx1. WRR4AOy-0 carries a C-terminal extension required for recognition of AcEx1, but reduces recognition of several effectors recognized by the WRR4ACol-0 allele. WRR4AOy-0 confers full resistance to AcEx1 when expressed in the oilseed crop Camelina sativa.

AB - The oomycete Albugo candida causes white rust of Brassicaceae, including vegetable and oilseed crops, and wild relatives such as Arabidopsis thaliana. Novel White Rust Resistance (WRR) genes from Arabidopsis enable new insights into plant/parasite co-evolution. WRR4A from Arabidopsis accession Columbia (Col-0) provides resistance to many but not all white rust races, and encodes a nucleotide-binding, leucine-rich repeat immune receptor. Col-0 WRR4A resistance is broken by AcEx1, an isolate of A. candida. We identified an allele of WRR4A in Arabidopsis accession Øystese-0 (Oy-0) and other accessions that confers full resistance to AcEx1. WRR4AOy-0 carries a C-terminal extension required for recognition of AcEx1, but reduces recognition of several effectors recognized by the WRR4ACol-0 allele. WRR4AOy-0 confers full resistance to AcEx1 when expressed in the oilseed crop Camelina sativa.

KW - Arabidopsis thaliana

KW - camelina

KW - crop protection

KW - effector recognition

KW - evolution

KW - immunity

KW - natural variation

KW - NLR

KW - resistance gene

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DO - 10.1111/tpj.15396

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SN - 0960-7412

VL - 107

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JO - Plant Journal

JF - Plant Journal

IS - 5

ER -

Evolutionary trade-offs at the Arabidopsis WRR4A resistance locus underpin alternate Albugo candida race recognition specificities

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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