A molecular roadmap to the plant immune system

Bentham, Adam R.; Concepcion, Juan Carlos De la; Mukhi, Nitika; ek, Rafa Zdrza; Draeger, Markus; Gorenkin, Danylo; Hughes, Richard K.; Banfield, Mark J.

doi:10.1074/jbc.rev120.010852

Cited by 90 publications

(40 citation statements)

References 266 publications

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“…To counteract these virulence factors, plants have evolved an array of intracellular immune receptors belonging to the nucleotide-binding, leucine-rich repeat (NLR) superfamily that can detect pathogen effectors [ 3 ]. Upon recognition, NLRs trigger the activation of immune responses that ultimately lead to localised programmed cell death, stopping the spread of the pathogen [ 4 , 5 ].…”

Section: Introductionmentioning

confidence: 99%

The allelic rice immune receptor Pikh confers extended resistance to strains of the blast fungus through a single polymorphism in the effector binding interface

et al. 2021

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Arms race co-evolution drives rapid adaptive changes in pathogens and in the immune systems of their hosts. Plant intracellular NLR immune receptors detect effectors delivered by pathogens to promote susceptibility, activating an immune response that halts colonization. As a consequence, pathogen effectors evolve to escape immune recognition and are highly variable. In turn, NLR receptors are one of the most diverse protein families in plants, and this variability underpins differential recognition of effector variants. The molecular mechanisms underlying natural variation in effector recognition by NLRs are starting to be elucidated. The rice NLR pair Pik-1/Pik-2 recognizes AVR-Pik effectors from the blast fungus Magnaporthe oryzae, triggering immune responses that limit rice blast infection. Allelic variation in a heavy metal associated (HMA) domain integrated in the receptor Pik-1 confers differential binding to AVR-Pik variants, determining resistance specificity. Previous mechanistic studies uncovered how a Pik allele, Pikm, has extended recognition to effector variants through a specialized HMA/AVR-Pik binding interface. Here, we reveal the mechanistic basis of extended recognition specificity conferred by another Pik allele, Pikh. A single residue in Pikh-HMA increases binding to AVR-Pik variants, leading to an extended effector response in planta. The crystal structure of Pikh-HMA in complex with an AVR-Pik variant confirmed that Pikh and Pikm use a similar molecular mechanism to extend their pathogen recognition profile. This study shows how different NLR receptor alleles functionally converge to extend recognition specificity to pathogen effectors.

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Section: Introductionmentioning

confidence: 99%

The allelic rice immune receptor Pikh confers extended resistance to strains of the blast fungus through a single polymorphism in the effector binding interface

et al. 2021

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“…Pathogens use an array of molecules, termed effectors, to successfully colonize hosts (Win et al, 2012). Intracellular detection of effectors relies on immune receptors from the nucleotide-binding, leucine-rich repeats (NLR) superfamily (Bentham et al, 2020; Jones et al, 2016; Saur et al, 2020). Upon recognition, NLRs act as nucleotide-operated switches, exchanging ADP for ATP (Bernoux et al, 2016; Tameling et al, 2002; Wang et al, 2019b; Williams et al, 2011), and oligomerise into supramolecular signalling platforms (Hu et al, 2015; Ma et al, 2020; Martin et al, 2020; Sharif et al, 2019; Tenthorey et al, 2017; Wang et al, 2019a; Zhang et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair

Concepcion

Benjumea

Bialas

et al. 2021

Preprint

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Cooperation between receptors from the NLR superfamily is important for intracellular activation of immune responses. NLRs can function in pairs that, upon pathogen recognition, trigger hypersensitive cell death and stop pathogen invasion. Natural selection drives specialization of host immune receptors towards an optimal response, whilst keeping a tight regulation of immunity in the absence of pathogens. However, the molecular basis of co-adaptation and specialization between paired NLRs remains largely unknown. Here, we describe functional specialization in alleles of the rice NLR pair Pik that confers resistance to strains of the blast fungus Magnaporthe oryzae harbouring AVR-Pik effectors. We revealed that matching pairs of allelic Pik NLRs mount effective immune responses whereas mismatched pairs lead to autoimmune phenotypes, a hallmark of hybrid necrosis in both natural and domesticated plant populations. We further showed that allelic specialization is largely underpinned by a single amino acid polymorphism that determines preferential association between matching pairs of Pik NLRs. These results provide a framework for how functionally linked immune receptors undergo co-adaptation to provide an effective and regulated immune response against pathogens. Understanding the molecular constraints that shape paired NLR evolution has implications beyond plant immunity given that hybrid necrosis can drive reproductive isolation.

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“…The active state of ZAR1 binds ATP and forms a pentameric resistosome that is proposed to function as a calcium channel . The canonical domains such as TIR, CC and NB-ARC and a few noncanonical domains from plant NLR immune receptors have also been structurally characterized (Bentham et al, 2020). The HMA domains of the Pikp-1, Pikm-1 and Pia NLRs and the WRKY domain of the RRS1 immune receptor have been structurally characterized (Maqbool et al, 2015;Ortiz et al, 2017;Zhang et al, 2017;De la Concepcion et al, 2018;Guo et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Expression, purification and crystallization of the N-terminal Solanaceae domain of the Sw-5b NLR immune receptor

Xin

Zhao

et al. 2021

Acta Cryst Sect F

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Plant nucleotide-binding domain and leucine-rich repeat receptors (NLRs) play crucial roles in recognizing pathogen effectors and activating plant immunity. The tomato NLR Sw-5b is a coiled-coil NLR (CC-NLR) immune receptor that confers resistance against tospoviruses, which cause serious economic losses in agronomic crops worldwide. Compared with other CC-NLRs, Sw-5b possesses an extended N-terminal Solanaceae domain (SD). The SD of Sw-5b is critical for recognition of the tospovirus viral movement protein NSm. An SD is also frequently detected in many NLRs from Solanaceae plants. However, no sequences homologous to the SD have been detected in animals or in plants other than Solanaceae. The properties of the SD protein are largely unknown, and thus 3D structural information is vital in order to better understand its role in pathogen perception and the activation of immune receptors. Here, the expression, purification and crystallization of Sw-5b SD (amino acids 1–245) are reported. Native and selenomethionine-substituted crystals of the SD protein belonged to space group P3112, with unit-cell parameters a = 81.53, b = 81.53, c = 98.44 Å and a = 81.63, b = 81.63, c = 98.80 Å, respectively. This is the first report of a structural study of the noncanonical SD domain of the NLR proteins from Solanaceae plants.

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A molecular roadmap to the plant immune system

Cited by 90 publications

References 266 publications

The allelic rice immune receptor Pikh confers extended resistance to strains of the blast fungus through a single polymorphism in the effector binding interface

The allelic rice immune receptor Pikh confers extended resistance to strains of the blast fungus through a single polymorphism in the effector binding interface

Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair

Expression, purification and crystallization of the N-terminal Solanaceae domain of the Sw-5b NLR immune receptor

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