Individual components of paired typical NLR immune receptors are regulated by distinct E3 ligases

Abstract

In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins serve as intracellular immune receptors. Defence signalling by NLRs often requires the formation of NLR heteropairs. Our knowledge of the molecular mechanism regulating this process is limited. In a reverse genetic screen to identify the partner of the Arabidopsis typical NLR, SUPRESSOR OF NPR1, CONSTITUTIVE 1 (SNC1), we discovered three NLRs that are redundantly required for SNC1-mediated defence, which were named SIDEKICK SNC1 1 (SIKIC1), SIKIC2 and SIKIC3. Immunoprecipitation-mass spectrometry analyses revealed that SIKIC2 physically associates with SNC1. We also uncovered that the protein level of SIKIC2 is under the control of two previously uncharacterized redundant E3 ubiquitin ligases MUSE1 and MUSE2. As SNC1 accumulation has previously been shown to be regulated by the E3 ubiquitin ligase SCF, this report provides evidence that the homeostasis of individual components of partnered typical NLRs is subjected to differential regulation via ubiquitin-mediated protein degradation.

The plant hypersensitive response: concepts, control and consequences

“…While this is still an active area of research, there is some evidence that specific E3 ligases are recruited to direct the degradation of specific NLRs (Huang et al , ). The regulation of NLR turnover by the ubiquitin‐mediated protein degradation system has been reviewed in detail elsewhere (Dong et al , ; Feechan et al , ).…”

Plant E3 ligases SNIPER 1 and SNIPER 2 broadly regulate the homeostasis of sensor NLR immune receptors

“…However, over‐accumulated NLRs could be detrimental to plant growth and development. Although some NLRs, such as SNC1, SIKIC1/2/3, RPS2, N, and MLAs, were reported to have their own regulatory E3 ligases (Cheng et al , ; Gou et al , ; Wang et al , ; Dong et al , ; Zhang et al , ), these specific E3s are less efficient in dampening such large‐scale immune up‐regulation. Usage of pathogen‐induced E3s like SNIPER1/2 would be more efficient to reduce global sNLRs levels to prevent autoimmunity.…”

“…The F‐box protein CPR1 is part of the SCF CPR1 complex E3 that targets two sNLRs, SNC1 and RPS2, for ubiquitination and degradation (Cheng et al , ; Gou et al , ). In parallel, two functionally redundant RING‐type E3 ligases, MUSE1 and MUSE2, are required for the turnover of SNC1's partners, SIKIC1/2/3 (Dong et al , ). These E3s show very narrow specificity in regard to substrate recognition.…”

The ubiquitin system affects agronomic plant traits

“…E3 ligases containing CPR1 likely also ubiquitinate a subset of other R proteins (118). An R protein that interacts with SNC1, SIKIC2 (SIDEKICK SNC1 2), is negatively regulated by two related and functionally redundant E3 ligases MUSE1 and MUSE 2 (MUTANT, SNC1-ENHANCING), distinct from the CUL1 CPR1 ligase (120). A double loss-of-function muse1 muse2 plant exhibits constitutive defense transcriptional responses, enhanced resistance, and severely stunted growth (120).…”

“…An R protein that interacts with SNC1, SIKIC2 (SIDEKICK SNC1 2), is negatively regulated by two related and functionally redundant E3 ligases MUSE1 and MUSE 2 (MUTANT, SNC1-ENHANCING), distinct from the CUL1 CPR1 ligase (120). A double loss-of-function muse1 muse2 plant exhibits constitutive defense transcriptional responses, enhanced resistance, and severely stunted growth (120). A strong autoimmune response is detected in a SIKIC2 over-expression line in the muse1 muse2 background.…”