Structural basis of pathogen recognition by an integrated HMA domain in a plant NLR immune receptor

Maqbool, Abbas; Saitoh, Hiromasa; Franceschetti, Marina; Stevenson, Clare E. M.; Uemura, Aiko; Kanzaki, Hiromitsu; Kamoun, Sophien; Terauchi, Ryohei; Banfield, Mark J.

doi:10.7554/elife.08709

Cited by 258 publications

(578 citation statements)

References 65 publications

(107 reference statements)

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“…This strategy is becoming more feasible as the crystal structure of the first IDeffector complex (i.e. Pik-1_HMA-AVR-Pik) was recently resolved, opening doors to the engineering of Pik-1 and RGA5 HMA domains for expanded effector recognition specificities (Maqbool et al, 2015). Although a promising strategy, ID engineering is challenging.…”

Section: How To Engineer Nlr-mediated Disease Resistance?mentioning

confidence: 99%

Multiple strategies for pathogen perception by plant immune receptors

2017

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Contents Summary17I.Introduction17II.Pathogen perception by NLRs: from direct recognition to integrated decoys18III.Multiple activation and signaling pathways for NLRs18IV.How to engineer NLR‐mediated disease resistance?21V.Conclusion23Acknowledgements23References23 Summary Plants have evolved a complex immune system to protect themselves against phytopathogens. A major class of plant immune receptors called nucleotide‐binding domain and leucine‐rich repeat‐containing proteins (NLRs) is ubiquitous in plants and is widely used for crop disease protection, making these proteins critical contributors to global food security. Until recently, NLRs were thought to be conserved in their modular architecture and functional features. Investigation of their biochemical, functional and structural properties has revealed fascinating mechanisms that enable these proteins to perceive a wide range of pathogens. Here, I review recent insights demonstrating that NLRs are more mechanistically and structurally diverse than previously thought. I also discuss how these findings provide exciting future prospects to improve plant disease resistance.

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Section: How To Engineer Nlr-mediated Disease Resistance?mentioning

confidence: 99%

Multiple strategies for pathogen perception by plant immune receptors

2017

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“…In these cases, the leucine-rich repeat domain plays a crucial role in recognition specificity and has frequently been shown to mediate direct effector binding (Ellis et al, 2007;Krasileva et al, 2010;Jia et al, 2000). Alternatively, direct effector recognition can be mediated by noncanonical domains integrated into NLRs at low frequencies (Kanzaki et al, 2012;Sarris et al, 2015;Maqbool et al, 2015;Le Roux et al, 2015;Césari et al, 2013). Recent work led to the hypothesis that these highly diverse integrated domains are mimics of effector targets and can therefore be considered as integrated decoy domains (Le Roux et al, 2015;Sarris et al, 2015;Césari et al, 2014a).…”

Section: Introductionmentioning

confidence: 99%

“…However, contrary to the C-terminal RATX1 domain of RGA5, the HMA domain of Pik-1 is located between the coiled-coil and nucleotide binding domains, indicating independent integration of the same domains in the two unrelated NLRs . Recently, the determination of the crystal structure of the AVR-PikD/Pikp-1 HMA domain complex allowed the precise identification of the AVR-PikD surface mediating binding to the Pikp-1 HMA domain (Maqbool et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Recognition of the Magnaporthe oryzae Effector AVR-Pia by the Decoy Domain of the Rice NLR Immune Receptor RGA5

et al. 2017

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Nucleotide binding domain and leucine-rich repeat proteins (NLRs) are important receptors in plant immunity that allow recognition of pathogen effectors. The rice (Oryza sativa) NLR RGA5 recognizes the Magnaporthe oryzae effector AVR-Pia through direct interaction. Here, we gained detailed insights into the molecular and structural bases of AVR-Pia-RGA5 interaction and the role of the RATX1 decoy domain of RGA5. NMR titration combined with in vitro and in vivo protein-protein interaction analyses identified the AVR-Pia interaction surface that binds to the RATX1 domain. Structure-informed AVR-Pia mutants showed that, although AVR-Pia associates with additional sites in RGA5, binding to the RATX1 domain is necessary for pathogen recognition but can be of moderate affinity. Therefore, RGA5-mediated resistance is highly resilient to mutations in the effector. We propose a model that explains such robust effector recognition as a consequence, and an advantage, of the combination of integrated decoy domains with additional independent effector-NLR interactions.

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“…To date, structure-guided studies of plant NLRs have been restricted to the N-terminal TIR or CC domain (6,14,17,26), with the exception of the noncanonical integrated-sensor heavy metalassociated domain from the rice NLR Pik (27). Although the plant NLR TIR domains have a conserved fold (6,17), the structures of the two known CC domain fragments from barley MLA10 and potato Rx are strikingly different.…”

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confidence: 99%

The CC domain structure from the wheat stem rust resistance protein Sr33 challenges paradigms for dimerization in plant NLR proteins

Casey

Lavrencic

Bentham

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

114

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Plants use intracellular immunity receptors, known as nucleotidebinding oligomerization domain-like receptors (NLRs), to recognize specific pathogen effector proteins and induce immune responses. These proteins provide resistance to many of the world's most destructive plant pathogens, yet we have a limited understanding of the molecular mechanisms that lead to defense signaling. We examined the wheat NLR protein, Sr33, which is responsible for strainspecific resistance to the wheat stem rust pathogen, Puccinia graminis f. sp. tritici. We present the solution structure of a coiled-coil (CC) fragment from Sr33, which adopts a four-helix bundle conformation. Unexpectedly, this structure differs from the published dimeric crystal structure of the equivalent region from the orthologous barley powdery mildew resistance protein, MLA10, but is similar to the structure of the distantly related potato NLR protein, Rx. We demonstrate that these regions are, in fact, largely monomeric and adopt similar folds in solution in all three proteins, suggesting that the CC domains from plant NLRs adopt a conserved fold. However, larger C-terminal fragments of Sr33 and MLA10 can self-associate both in vitro and in planta, and this self-association correlates with their cell death signaling activity. The minimal region of the CC domain required for both cell death signaling and self-association extends to amino acid 142, thus including 22 residues absent from previous biochemical and structural protein studies. These data suggest that self-association of the minimal CC domain is necessary for signaling but is likely to involve a different structural basis than previously suggested by the MLA10 crystallographic dimer.plant innate immunity | resistance protein | NLR proteins | effectortriggered immunity | nuclear magnetic resonance spectroscopy

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Structural basis of pathogen recognition by an integrated HMA domain in a plant NLR immune receptor

Cited by 258 publications

References 65 publications

Multiple strategies for pathogen perception by plant immune receptors

Multiple strategies for pathogen perception by plant immune receptors

Recognition of the Magnaporthe oryzae Effector AVR-Pia by the Decoy Domain of the Rice NLR Immune Receptor RGA5

The CC domain structure from the wheat stem rust resistance protein Sr33 challenges paradigms for dimerization in plant NLR proteins

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