Distinct modes of derepression of an Arabidopsis immune receptor complex by two different bacterial effectors

Yan Ma, Hailong Guo, Lanxi Hu, Paula Pons Martinez, Panagiotis N Moschou, Volkan Cevik, Pingtao Ding, Zane Duxbury, Panagiotis F Sarris, Jonathan D G Jones

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Plant intracellular nucleotide-binding leucine-rich repeat (NLR) immune receptors often function in pairs to detect pathogen effectors and activate defense. The Arabidopsis RRS1-R-RPS4 NLR pair recognizes the bacterial effectors AvrRps4 and PopP2 via an integrated WRKY transcription factor domain in RRS1-R that mimics the effector's authentic targets. How the complex activates defense upon effector recognition is unknown. Deletion of the WRKY domain results in an RRS1 allele that triggers constitutive RPS4-dependent defense activation, suggesting that in the absence of effector, the WRKY domain contributes to maintaining the complex in an inactive state. We show the WRKY domain interacts with the adjacent domain 4, and that the inactive state of RRS1 is maintained by WRKY-domain 4 interactions before ligand detection. AvrRps4 interaction with the WRKY domain disrupts WRKY-domain 4 association, thus derepressing the complex. PopP2-triggered activation is less easily explained by such disruption and involves the longer C-terminal extension of RRS1-R. Furthermore, some mutations in RPS4 and RRS1 compromise PopP2 but not AvrRps4 recognition, suggesting that AvrRps4 and PopP2 derepress the complex differently. Consistent with this, a "reversibly closed" conformation of RRS1-R, engineered in a method exploiting the high affinity of colicin E9 and Im9 domains, reversibly loses AvrRps4, but not PopP2 responsiveness. Following RRS1 derepression, interactions between domain 4 and the RPS4 C-terminal domain likely contribute to activation. Simultaneous relief of autoinhibition and activation may contribute to defense activation in many immune receptors.

LanguageEnglish
Pages10218-10227
Number of pages10
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number41
Early online date25 Sep 2018
DOIs
StatusPublished - 9 Oct 2018

Fingerprint

Antigen-Antibody Complex
Leucine
Nucleotides
Colicins
Arabidopsis
Transcription Factors
Alleles
Ligands
Mutation

Keywords

  • Effector target
  • Effector-triggered immunity
  • Integrated decoy
  • Paired NLR immune receptors
  • Plant-disease resistance

ASJC Scopus subject areas

  • General

Cite this

Distinct modes of derepression of an Arabidopsis immune receptor complex by two different bacterial effectors. / Ma, Yan; Guo, Hailong; Hu, Lanxi; Martinez, Paula Pons; Moschou, Panagiotis N; Cevik, Volkan; Ding, Pingtao; Duxbury, Zane; Sarris, Panagiotis F; Jones, Jonathan D G.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 41, 09.10.2018, p. 10218-10227.

Research output: Contribution to journalArticle

Ma, Yan ; Guo, Hailong ; Hu, Lanxi ; Martinez, Paula Pons ; Moschou, Panagiotis N ; Cevik, Volkan ; Ding, Pingtao ; Duxbury, Zane ; Sarris, Panagiotis F ; Jones, Jonathan D G. / Distinct modes of derepression of an Arabidopsis immune receptor complex by two different bacterial effectors. In: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Vol. 115, No. 41. pp. 10218-10227.
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AU - Cevik, Volkan

AU - Ding, Pingtao

AU - Duxbury, Zane

AU - Sarris, Panagiotis F

AU - Jones, Jonathan D G

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