Structural and Functional Analysis of a Plant Resistance Protein TIR Domain Reveals Interfaces for Self-Association, Signaling, and Autoregulation

Bernoux, Maud; Ve, Thomas; Williams, Simon J.; Warren, Christopher L.; Hatters, Danny M.; Valkov, Eugene; Zhang, Xiaoxiao; Ellis, Jeffrey G.; Kobe, Boštjan; Dodds, Peter N.

doi:10.1016/j.chom.2011.02.009

Cited by 327 publications

(425 citation statements)

References 64 publications

(87 reference statements)

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“…Many lines of evidence suggest TIR-TIR interactions are important for TNL function 24,37 . The TIR domains of RRS1 and RPS4 interact in a yeast two hybrid assay and associate in planta after co-IP 24 .…”

Section: Resultsmentioning

confidence: 99%

Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4

et al. 2015

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Plant immunity requires recognition of pathogen effectors by intracellular NB-LRR immune receptors encoded by Resistance (R) genes. Most R proteins recognize a specific effector, but some function in pairs that recognize multiple effectors. Arabidopsis thaliana TIR-NB-LRR proteins RRS1-R and RPS4 together recognize two bacterial effectors, AvrRps4 from Pseudomonas syringae and PopP2 from Ralstonia solanacearum. However, AvrRps4, but not PopP2, is recognized in rrs1/rps4 mutants. We reveal an R gene pair that resembles and is linked to RRS1/RPS4, designated as RRS1B/RPS4B, which confers recognition of AvrRps4 but not PopP2. Like RRS1/RPS4, RRS1B/RPS4B proteins associate and activate defence genes upon AvrRps4 recognition. Inappropriate combinations (RRS1/RPS4B or RRS1B/RPS4) are non-functional and this specificity is not TIR domain dependent. Distinct putative orthologues of both pairs are maintained in the genomes of Arabidopsis thaliana relatives and are likely derived from a common ancestor pair. Our results provide novel insights into paired R gene function and evolution.

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Section: Resultsmentioning

confidence: 99%

Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4

et al. 2015

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“…The recent elucidation of the structures of the CC domain of MLA and the TIR domain of L6, a resistance protein against flax rust, both shown to form homodimers, has led to renewed attention for the role of self-association in the functioning of R proteins (Bernoux et al, 2011;Maekawa et al, 2011a). Multimerization via the NB-ARC domain after activation is a common theme in proteins belonging to the STAND clade (Danot et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

“…7C, 5). In case of Rx1, it was shown that the NB domain itself can initiate a cell death response in the absence of the other domains (Rairdan et al, 2008), but for several other NB-LRR R proteins, the Nterminal CC or TIR domain has signaling capabilities (Swiderski et al, 2009;Bernoux et al, 2011;Collier et al, 2011;Maekawa et al, 2011a). The electrostatic attraction between the conserved clusters of charged residues on the ARC2 and LRR is predicted to facilitate the reassociation of the domains when the R protein completes the activation cycle and returns to its resting state (Fig.…”

Section: Discussionmentioning

confidence: 99%

Structural Determinants at the Interface of the ARC2 and Leucine-Rich Repeat Domains Control the Activation of the Plant Immune Receptors Rx1 and Gpa2

et al. 2013

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Many plant and animal immune receptors have a modular nucleotide-binding-leucine-rich repeat (NB-LRR) architecture in which a nucleotide-binding switch domain, NB-ARC, is tethered to a LRR sensor domain. The cooperation between the switch and sensor domains, which regulates the activation of these proteins, is poorly understood. Here, we report structural determinants governing the interaction between the NB-ARC and LRR in the highly homologous plant immune receptors Gpa2 and Rx1, which recognize the potato cyst nematode Globodera pallida and Potato virus X, respectively. Systematic shuffling of polymorphic sites between Gpa2 and Rx1 showed that a minimal region in the ARC2 and N-terminal repeats of the LRR domain coordinate the activation state of the protein. We identified two closely spaced amino acid residues in this region of the ARC2 (positions 401 and 403) that distinguish between autoactivation and effector-triggered activation. Furthermore, a highly acidic loop region in the ARC2 domain and basic patches in the N-terminal end of the LRR domain were demonstrated to be required for the physical interaction between the ARC2 and LRR. The NB-ARC and LRR domains dissociate upon effector-dependent activation, and the complementary-charged regions are predicted to mediate a fast reassociation, enabling multiple rounds of activation. Finally, we present a mechanistic model showing how the ARC2, NB, and N-terminal half of the LRR form a clamp, which regulates the dissociation and reassociation of the switch and sensor domains in NB-LRR proteins.Resistance (R) proteins play a central role in the recognition-based immune system of plants. Unlike vertebrates, plants lack an adaptive immune system with highly specialized immune cells. Instead, they rely on an innate immune system in which each cell is autonomous. Two types of immune receptors can be distinguished in plants, pathogen-associated molecular patterns recognition receptors that detect conserved molecular patterns in plant pathogens and intracellular R proteins that recognize specific effectors employed by pathogens as modifiers of host metabolism or defense mechanisms (Jones and Dangl, 2006). Effector-triggered activation of R proteins leads to an array of protective responses, often culminating in programmed cell death at the site of infection (Greenberg and Yao, 2004), thereby preventing further ingress of the pathogen. Pathogens have evolved mechanisms to evade recognition by R proteins and to regain their virulence (Dodds and Rathjen, 2010). This continuous coevolutionary process between host and pathogen has resulted in a reservoir of highly diverse R proteins in plants, enabling them to counteract a wide range of pathogens and pests.The most common class of R proteins consists of nucleotide-binding (NB)-leucine-rich repeat (LRR) proteins with a tripartite domain architecture, which roughly corresponds to an N-terminal response domain (a coiled coil [CC] or Toll/Interleukin-1 receptor [TIR] domain) involved in downstream signaling, a central molecula...

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“…Expression of the N-terminal regions from several TIR-NB-LRRs has been previously reported to induce cell death (Frost et al, 2004;Weaver et al, 2006;Swiderski et al, 2009;Krasileva et al, 2010;Bernoux et al, 2011), suggesting that TIR domains are involved in defense signaling. We have reported that the N-terminal CC R domains of NRG1 and ADR1 also induce cell death (Collier et al, 2011).…”

Section: Discussion Activation Of Cell Death By the CC Domains Of I2-mentioning

confidence: 99%

“…In many cases, recognition of pathogens is mediated through plant recognition co-factors that interact both with the N-terminal TIR or CC domain of an NB-LRR and the cognate effector protein (Collier and Moffett, 2009;Saunders et al, 2012;Lewis et al, 2013). Expression of the N-terminal domains of some NB-LRRs has also been shown to induce cell death, including TIR (Frost et al, 2004;Weaver et al, 2006;Swiderski et al, 2009;Krasileva et al, 2010;Bernoux et al, 2011), CC (Maekawa et al, 2011;Wang et al, 2015), and CC R (Collier et al, 2011) domains. These observations have led to the question of whether the N termini of NB-LRR proteins are involved in pathogen recognition, signaling, or both.…”

mentioning

confidence: 99%

The Chloroplastic Protein THF1 Interacts with the Coiled-Coil Domain of the Disease Resistance Protein N′ and Regulates Light-Dependent Cell Death

et al. 2016

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One branch of plant immunity is mediated through nucleotide-binding/Leu-rich repeat (NB-LRR) family proteins that recognize specific effectors encoded by pathogens. Members of the I2-like family constitute a well-conserved subgroup of NB-LRRs from Solanaceae possessing a coiled-coil (CC) domain at their N termini. We show here that the CC domains of several I2-like proteins are able to induce a hypersensitive response (HR), a form of programmed cell death associated with disease resistance. Using yeast two-hybrid screens, we identified the chloroplastic protein Thylakoid Formation1 (THF1) as an interacting partner for several I2-like CC domains. Co-immunoprecipitations and bimolecular fluorescence complementation assays confirmed that THF1 and I2-like CC domains interact in planta and that these interactions take place in the cytosol. Several HR-inducing I2-like CC domains have a negative effect on the accumulation of THF1, suggesting that the latter is destabilized by active CC domains. To confirm this model, we investigated N9, which recognizes the coat protein of most Tobamoviruses, as a prototypical member of the I2-like family. Transient expression and gene silencing data indicated that THF1 functions as a negative regulator of cell death and that activation of full-length N9 results in the destabilization of THF1. Consistent with the known function of THF1 in maintaining chloroplast homeostasis, we show that the HR induced by N9 is light-dependent. Together, our results define, to our knowledge, novel molecular mechanisms linking light and chloroplasts to the induction of cell death by a subgroup of NB-LRR proteins.

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Structural and Functional Analysis of a Plant Resistance Protein TIR Domain Reveals Interfaces for Self-Association, Signaling, and Autoregulation

Cited by 327 publications

References 64 publications

Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4

Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4

Structural Determinants at the Interface of the ARC2 and Leucine-Rich Repeat Domains Control the Activation of the Plant Immune Receptors Rx1 and Gpa2

The Chloroplastic Protein THF1 Interacts with the Coiled-Coil Domain of the Disease Resistance Protein N′ and Regulates Light-Dependent Cell Death

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