The nuclear immune receptor RPS4 is required for RRS1SLH1-dependent constitutive defense activation in Arabidopsis thaliana

Kee Hoon Sohn, Cécile Segonzac, Ghanasyam Rallapalli, Panagiotis F. Sarris, Joo Yong Woo, Simon J. Williams, Toby E. Newman, Kyung Hee Paek, Bostjan Kobe, Jonathan D.G. Jones

Research output: Contribution to journalArticle

44 Citations (Scopus)

Abstract

Plant nucleotide-binding leucine-rich repeat (NB-LRR) disease resistance (R) proteins recognize specific "avirulent" pathogen effectors and activate immune responses. NB-LRR proteins structurally and functionally resemble mammalian Nod-like receptors (NLRs). How NB-LRR and NLR proteins activate defense is poorly understood. The divergently transcribed Arabidopsis R genes, RPS4 (resistance to Pseudomonas syringae 4) and RRS1 (resistance to Ralstonia solanacearum 1), function together to confer recognition of Pseudomonas AvrRps4 and Ralstonia PopP2. RRS1 is the only known recessive NB-LRR R gene and encodes a WRKY DNA binding domain, prompting suggestions that it acts downstream of RPS4 for transcriptional activation of defense genes. We define here the early RRS1-dependent transcriptional changes upon delivery of PopP2 via Pseudomonas type III secretion. The Arabidopsis slh1 (sensitive to low humidity 1) mutant encodes an RRS1 allele (RRS1SLH1) with a single amino acid (leucine) insertion in the WRKY DNA-binding domain. Its poor growth due to constitutive defense activation is rescued at higher temperature. Transcription profiling data indicate that RRS1SLH1-mediated defense activation overlaps substantially with AvrRps4- and PopP2-regulated responses. To better understand the genetic basis of RPS4/RRS1-dependent immunity, we performed a genetic screen to identify suppressor of slh1 immunity (sushi) mutants. We show that many sushi mutants carry mutations in RPS4, suggesting that RPS4 acts downstream or in a complex with RRS1. Interestingly, several mutations were identified in a domain C-terminal to the RPS4 LRR domain. Using an Agrobacterium-mediated transient assay system, we demonstrate that the P-loop motif of RPS4 but not of RRS1SLH1 is required for RRS1SLH1 function. We also recapitulate the dominant suppression of RRS1SLH1 defense activation by wild type RRS1 and show this suppression requires an intact RRS1 P-loop. These analyses of RRS1SLH1 shed new light on mechanisms by which NB-LRR protein pairs activate defense signaling, or are held inactive in the absence of a pathogen effector.

Original languageEnglish
Pages (from-to)e1004655
JournalPLoS Genetics
Volume10
Issue number10
DOIs
Publication statusPublished - 2014 Oct 1

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Ralstonia solanacearum
Pseudomonas syringae
Cytoplasmic and Nuclear Receptors
Arabidopsis
Arabidopsis thaliana
leucine
immunity
Nucleotides
Leucine
nucleotides
protein
vpr Genes
Immunity
DNA-binding domains
gene
mutation
humidity
pathogen
Humidity
Pseudomonas

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Sohn, K. H., Segonzac, C., Rallapalli, G., Sarris, P. F., Woo, J. Y., Williams, S. J., ... Jones, J. D. G. (2014). The nuclear immune receptor RPS4 is required for RRS1SLH1-dependent constitutive defense activation in Arabidopsis thaliana. PLoS Genetics, 10(10), e1004655. https://doi.org/10.1371/journal.pgen.1004655

The nuclear immune receptor RPS4 is required for RRS1SLH1-dependent constitutive defense activation in Arabidopsis thaliana. / Sohn, Kee Hoon; Segonzac, Cécile; Rallapalli, Ghanasyam; Sarris, Panagiotis F.; Woo, Joo Yong; Williams, Simon J.; Newman, Toby E.; Paek, Kyung Hee; Kobe, Bostjan; Jones, Jonathan D.G.

In: PLoS Genetics, Vol. 10, No. 10, 01.10.2014, p. e1004655.

Research output: Contribution to journalArticle

Sohn, KH, Segonzac, C, Rallapalli, G, Sarris, PF, Woo, JY, Williams, SJ, Newman, TE, Paek, KH, Kobe, B & Jones, JDG 2014, 'The nuclear immune receptor RPS4 is required for RRS1SLH1-dependent constitutive defense activation in Arabidopsis thaliana', PLoS Genetics, vol. 10, no. 10, pp. e1004655. https://doi.org/10.1371/journal.pgen.1004655
Sohn, Kee Hoon ; Segonzac, Cécile ; Rallapalli, Ghanasyam ; Sarris, Panagiotis F. ; Woo, Joo Yong ; Williams, Simon J. ; Newman, Toby E. ; Paek, Kyung Hee ; Kobe, Bostjan ; Jones, Jonathan D.G. / The nuclear immune receptor RPS4 is required for RRS1SLH1-dependent constitutive defense activation in Arabidopsis thaliana. In: PLoS Genetics. 2014 ; Vol. 10, No. 10. pp. e1004655.
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