The Integrated LIM-Peptidase Domain of the CSA1/CHS3 Paired Immune Receptor Detects Changes in DA1 Family Peptidase Inhibitors in Arabidopsis

Gu, Benguo; Parkes, Toby; Smith, Caroline; Lu, Fu-Hao; McKenzie, Neil; Dong, Hui; Jones, Jimmy; Çevik, Volkan; Bevan, Michael W.

doi:10.2139/ssrn.4167271

Cited by 3 publications

(3 citation statements)

References 22 publications

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“…Fourth, the E3 ligases BB (30) and DA2, which ubiquitinate DA1, are characterized by a high turnover. Fifth, DAR3 inhibits the activity of DA1 to repress endoreduplication (89). Last, by directly deubiquitinating DA2 and hereby limiting its ubiquitination activity toward DA1, UBP12 and UBP13 further limit the ubiquitination of DA1 and its related proteins (Fig.…”

Section: Ubp12 and Ubp13 Regulate Growth By Limiting The Activity Of ...mentioning

confidence: 99%

A dynamic ubiquitination balance of cell proliferation and endoreduplication regulators determines plant organ size

Chen,

Vermeersch,

Van Leene

et al. 2024

Sci. Adv.

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Ubiquitination plays a crucial role throughout plant growth and development. The E3 ligase DA2 has been reported to activate the peptidase DA1 by ubiquitination, hereby limiting cell proliferation. However, the molecular mechanisms that regulate DA2 remain elusive. Here, we demonstrate that DA2 has a very high turnover and auto-ubiquitinates with K48-linkage polyubiquitin chains, which is counteracted by two deubiquitinating enzymes, UBIQUITIN-SPECIFIC PROTEASE 12 (UBP12) and UBP13. Unexpectedly, we found that auto-ubiquitination of DA2 does not influence its stability but determines its E3 ligase activity. We also demonstrate that impairing the protease activity of DA1 abolishes the growth-reducing effect of DA2. Last, we show that synthetic, constitutively activated DA1-ubiquitin fusion proteins overrule this complex balance of ubiquitination and deubiquitination and strongly restrict growth and promote endoreduplication. Our findings highlight a nonproteolytic function of K48-linked polyubiquitination and reveal a mechanism by which DA2 auto-ubiquitination levels, in concert with UBP12 and UBP13, precisely monitor the activity of DA1 and fine-tune plant organ size.

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Section: Ubp12 and Ubp13 Regulate Growth By Limiting The Activity Of ...mentioning

confidence: 99%

A dynamic ubiquitination balance of cell proliferation and endoreduplication regulators determines plant organ size

Chen,

Vermeersch,

Van Leene

et al. 2024

Sci. Adv.

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“…Several functionally characterized NLR-IDs require another genetically linked canonical NLR to work in pairs for their function and are therefore known as NLR pairs (or sensor-executor pairs) 3,10 . Sensor and executor NLRs form pre-activation complexes in the resting state and, upon binding of effectors to the integrated domains, sensor NLRs undergo a series of intra-and intermolecular conformational rearrangements that relay effector perception to the executor NLRs for immune signaling initiation [11][12][13] . The Arabidopsis RRS1/RPS4 immune receptor complex, one of the best-studied paired NLRs, confers resistance to bacterial pathogens Pseudomonas syringae pv.…”

Section: Introductionmentioning

confidence: 99%

Reversible ubiquitination of integrated domain controls paired NLR immune receptor complex homeostasis

Chen,

Huang,

et al. 2024

Preprint

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Plant intracellular NLR immune receptors can function individually or in pairs to detect pathogen effectors and activate immune responses. NLR homeostasis has to be tightly regulated to ensure proper defense without triggering autoimmunity. However, in contrast to singleton NLRs, the mechanisms controlling the paired NLRs complex homeostasis are less understood. The paired Arabidopsis RRS1/RPS4 immune receptor complex confers disease resistance through effector recognition mediated by the integrated WRKY domain of RRS1. Here, through proximity labelling, we reveal a ubiquitination-deubiquitination cycle that controls the homeostasis of the RRS1/RPS4 complex. E3 ligase RARE directly binds and ubiquitinates RRS1’s WRKY domain to promote its proteasomal degradation, thereby destabilizing RPS4 indirectly and compromising the stability and function of the RRS1/RPS4 complex. Conversely, the deubiquitinating enzymes UBP12/UBP13 deubiquitinate RRS1’s WRKY domain, counteracting RARE’s effects. Interestingly, the abundance of WRKY transcription factors WRKY70 and WRKY41 is also regulated by RARE and UBP12/UBP13. Phylogenetic analysis suggests this regulation likely transferred from WRKY70/WRKY41 to RRS1 upon WRKY domain integration. Our findings improve our understanding of homeostatic regulation of paired NLR complex and uncover a new paradigm whereby domain integration can co-opt preexisting post-translational modification to regulate novel protein functions.

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“…These IDs often mimic the host targets of effectors (Cesari et al , 2014; Kroj et al , 2016; Sarris et al , 2016). Within the NLR, IDs can be involved in effector sensing, either via direct or indirect recognition (Fujisaki et al , 2015; Maqbool et al , 2015; De la Concepcion et al , 2018; Gu et al , 2023). The integrated decoy hypothesis postulates that over evolutionary time, host targets of effectors have genetically integrated within NLRs, baiting pathogen effectors to activate host immunity (Cesari et al , 2014).…”

Section: Introductionmentioning

confidence: 99%

NLR receptors in plant immunity: making sense of the alphabet soup

Contreras,

Lüdke,

Pai

et al. 2023

EMBO Reports

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Plants coordinately use cell‐surface and intracellular immune receptors to perceive pathogens and mount an immune response. Intracellular events of pathogen recognition are largely mediated by immune receptors of the nucleotide binding and leucine rich‐repeat (NLR) classes. Upon pathogen perception, NLRs trigger a potent broad‐spectrum immune reaction, usually accompanied by a form of programmed cell death termed the hypersensitive response. Some plant NLRs act as multifunctional singleton receptors which combine pathogen detection and immune signaling. However, NLRs can also function in higher order pairs and networks of functionally specialized interconnected receptors. In this article, we cover the basic aspects of plant NLR biology with an emphasis on NLR networks. We highlight some of the recent advances in NLR structure, function, and activation and discuss emerging topics such as modulator NLRs, pathogen suppression of NLRs, and NLR bioengineering. Multi‐disciplinary approaches are required to disentangle how these NLR immune receptor pairs and networks function and evolve. Answering these questions holds the potential to deepen our understanding of the plant immune system and unlock a new era of disease resistance breeding.

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The Integrated LIM-Peptidase Domain of the CSA1/CHS3 Paired Immune Receptor Detects Changes in DA1 Family Peptidase Inhibitors in Arabidopsis

Cited by 3 publications

References 22 publications

A dynamic ubiquitination balance of cell proliferation and endoreduplication regulators determines plant organ size

A dynamic ubiquitination balance of cell proliferation and endoreduplication regulators determines plant organ size

Reversible ubiquitination of integrated domain controls paired NLR immune receptor complex homeostasis

NLR receptors in plant immunity: making sense of the alphabet soup

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