The Arabidopsis WRR4A and WRR4B  paralogous NLR proteins both confer recognition of multiple Albugo candida effectors

Amey Redkar, Volkan Cevik, Kate Bailey, He Zhao, Dae Sung Kim, Zhou Zou, Oliver J. Furzer, Sebastian Fairhead, M. Hossein Borhan, Eric B. Holub, Jonathan D.G. Jones

Research output: Contribution to journalArticlepeer-review

7 Citations (SciVal)

Abstract

The oomycete Albugo candida causes white blister rust, an important disease of Brassica crops. Distinct races of A. candida are defined by their capacity to infect different host plant species. Each A. candida race encodes secreted proteins with a CX2CX5G (‘CCG’) motif that are polymorphic and show presence/absence variation, and are therefore candidate effectors. The White Rust Resistance 4 (WRR4) locus in Arabidopsis thaliana accession Col-0 contains three genes that encode intracellular nucleotide-binding domain leucine-rich repeat immune receptors. The Col-0 alleles of WRR4A and WRR4B confer resistance to multiple A. candida races, although both WRR4A and WRR4B can be overcome by the Col-0-virulent race 4 isolate AcEx1. Comparison of CCG candidate effectors in avirulent and virulent races, and transient co-expression of CCG effectors from four A. candida races in Nicotiana sp. or A. thaliana, revealed CCG effectors that trigger WRR4A- or WRR4B-dependent hypersensitive responses. We found eight WRR4A-recognised CCGs and four WRR4B-recognised CCGs, the first recognised proteins from A. candida for which the cognate immune receptors in A. thaliana are known. This multiple recognition capacity potentially explains the broad-spectrum resistance to several A. candida races conferred by WRR4 paralogues. We further show that of five tested CCGs, three confer enhanced disease susceptibility when expressed in planta, consistent with A. candida CCG proteins being effectors.

Original languageEnglish
Pages (from-to)532-547
Number of pages16
JournalNew Phytologist
Volume237
Issue number2
Early online date7 Aug 2022
DOIs
Publication statusPublished - 31 Jan 2023

Bibliographical note

Funding Information:
AR acknowledges support by EMBO LTF (ALTF‐842‐2015). VC, OJF and SF were supported by Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/L011646/1. DSK, KB and JDGJ were supported in part by an ERC Advanced Investigator grant to JDGJ ‘ALBUGON’ Project ID 233376. Research in the Jones Laboratory is supported by the Gatsby Foundation (UK) and BBSRC.

Keywords

  • Albugo candida
  • Arabidopsis
  • effectors
  • hypersensitive response
  • oomycete
  • recognition
  • TIR–NLR
  • WRR4

ASJC Scopus subject areas

  • Physiology
  • Plant Science

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