A disease resistance protein triggers oligomerization of its NLR helper into a hexameric resistosome to mediate innate immunity DOI Creative Commons
Jogi Madhuprakash, AmirAli Toghani, Mauricio P. Contreras

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: June 19, 2024

Abstract NRCs are essential helper NLR (nucleotide-binding domain and leucine-rich repeat) proteins that execute the immune response triggered by disease resistance proteins, also known as sensor NLRs. The structure of resting state NbNRC2 was recently revealed to be a homodimer. However, sensor-activated has not yet been elucidated. In this study, we used cryo-EM determine NbNRC2, which forms hexameric inflammasome-like resistosome. To confirm functional significance hexamer, mutagenized interfaces involved in oligomerization found mutations three nucleotide-binding interface residues abolish signalling. Comparative structural analyses between homodimer homohexamer significant rearrangements before after activation, providing insights into activation mechanisms. Furthermore, comparisons hexamer previously reported CC-NLR pentameric assemblies features allow for integration an additional protomer. We assess released AlphaFold 3 prediction activated oligomers. This allows high-confidence modelling N-terminal α 1-helices other CC-NLRs, region proven difficult fully resolve using approaches. Overall, our work sheds light on biochemical mechanisms underpinning expands understanding diversity.

Language: Английский

Orthologous genes Pm12 and Pm21 from two wild relatives of wheat show evolutionary conservation but divergent powdery mildew resistance DOI Creative Commons
Shanying Zhu, Cheng Liu,

Shuangjun Gong

et al.

Plant Communications, Journal Year: 2022, Volume and Issue: 4(2), P. 100472 - 100472

Published: Nov. 9, 2022

Wheat powdery mildew, caused by Blumeria graminis f. sp. tritici (Bgt), is a devastating disease that threatens wheat production worldwide. Pm12, which originated from Aegilops speltoides, wild relative of wheat, confers strong resistance to mildew and therefore has potential use in breeding. Using susceptible mutants induced gamma irradiation, we physically mapped isolated Pm12 showed it be orthologous Pm21 Dasypyrum villosum, also wheat. The function was validated via ethyl methanesulfonate mutagenesis, virus-induced gene silencing, stable genetic transformation. Evolutionary analysis indicates the Pm12/Pm21 loci species are relatively conserved but dynamic. Here, demonstrated two genes, Pm21, possess differential against same set Bgt isolates. Overexpression coiled-coil domains both PM12 PM21 induces cell death Nicotiana benthamiana leaves. However, their full-length forms display different death-inducing activities distinct intramolecular interactions. Cloning will facilitate its application breeding programs. This study gives new insight into show race specificities interaction patterns.

Language: Английский

Citations

43
Wheat adaptation to environmental stresses under climate change: Molecular basis and genetic improvement DOI Creative Commons
Hude Mao, Cong Jiang, Chunlei Tang

et al.

Molecular Plant, Journal Year: 2023, Volume and Issue: 16(10), P. 1564 - 1589

Published: Sept. 9, 2023

Language: Английский

Citations

42
Structural polymorphisms within a common powdery mildew effector scaffold as a driver of coevolution with cereal immune receptors DOI Creative Commons
Yu Cao, Florian Kümmel, Elke Logemann

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(32)

Published: July 31, 2023

In plants, host-pathogen coevolution often manifests in reciprocal, adaptive genetic changes through variations host nucleotide-binding leucine-rich repeat immune receptors (NLRs) and virulence-promoting pathogen effectors. grass powdery mildew (PM) fungi, an extreme expansion of a RNase-like effector family, termed RALPH, dominates the repertoire, with some members recognized as avirulence (AVR) effectors by cereal NLR receptors. We report structures sequence-unrelated barley PM AVR

Language: Английский

Citations

34
Plasma membrane association and resistosome formation of plant helper immune receptors DOI Creative Commons

Zaiqing Wang,

Xiaoxiao Liu, Jie Yu

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(32)

Published: July 31, 2023

Intracellular plant immune receptors, termed NLRs (Nucleotide-binding Leucine-rich repeat Receptors), confer effector-triggered immunity. Sensor are responsible for pathogen effector recognition. Helper function downstream of sensor to transduce signaling and induce cell death Activation that contain TIR (Toll/interleukin-1receptor) domains generates small molecules an association between a heterodimer signalosome EDS1 (EnhancedDisease Susceptibility 1)/SAG101 (Senescence-AssociatedGene 101) the helper NLR NRG1 (NRequired Gene 1). Autoactive NRG1s oligomerize form calcium channels largely localized at plasma membrane (PM). The molecular mechanisms PM effector-induced oligomerization not well characterized. We demonstrate require positively charged residues in their N-terminal phospholipid binding before after activation, despite conformational changes accompany activation. activation TIR-containing induces cytoplasmic pool EDS1/SAG101 is critical function. cannot be detected oligomerized resistosome, suggesting additional unknown triggers might required dissociation from previously described NRG1/EDS1/SAG101 heterotrimer subsequent oligomerization. Alternatively, resulting abrogate interface association. Our data provide observations regarding dynamic during underpin updated model resistosome formation.

Language: Английский

Citations

33
Altering Specificity and Autoactivity of Plant Immune Receptors Sr33 and Sr50 Via a Rational Engineering Approach DOI Creative Commons
Janina Tamborski, Kyungyong Seong, Furong Liu

et al.

Molecular Plant-Microbe Interactions, Journal Year: 2023, Volume and Issue: 36(7), P. 434 - 446

Published: March 3, 2023

Many resistance genes deployed against pathogens in crops are intracellular nucleotide-binding (NB) leucine-rich repeat (LRR) receptors (NLRs). The ability to rationally engineer the specificity of NLRs will be crucial response newly emerging crop diseases. Successful attempts modify NLR recognition have been limited untargeted approaches or depended on previously available structural information knowledge pathogen-effector targets. However, this is not for most NLR-effector pairs. Here, we demonstrate precise prediction and subsequent transfer residues involved effector between two closely related without their experimentally determined structure detailed about pathogen By combining phylogenetics, allele diversity analysis, modeling, successfully predicted mediating interaction Sr50 with its cognate AvrSr50 transferred Sr33. We created synthetic versions Sr33 that contain amino acids from Sr50, including Sr33syn, which gained recognize 12 amino-acid substitutions. Furthermore, discovered sites LRR domain needed also influence autoactivity Sr50. Structural modeling suggests these interact a part NB-ARC domain, named latch, possibly maintain inactive state receptor. Our approach demonstrates rational modifications NLRs, could useful enhance existing elite germplasm. [Formula: see text] Copyright © 2023 Author(s). This an open access article distributed under CC BY-NC-ND 4.0 International license.

Language: Английский

Citations

31
New Biochemical Principles for NLR Immunity in Plants DOI Creative Commons
Jijie Chai, Wen Song, Jane E. Parker

et al.

Molecular Plant-Microbe Interactions, Journal Year: 2023, Volume and Issue: 36(8), P. 468 - 475

Published: Aug. 1, 2023

While working for the United States Department of Agriculture on North Dakota Agricultural College campus in Fargo, Dakota, 1940s and 1950s, Harold H. Flor formulated genetic principles coevolving plant host-pathogen interactions that govern disease resistance or susceptibility. His ‘gene-for-gene’ legacy runs deep modern pathology continues to inform molecular models immune recognition signaling. In this review, we discuss recent biochemical insights immunity conferred by nucleotide-binding domain/leucine-rich-repeat (NLR) receptors, which are major gene-for-gene determinants nature cultivated crops. Structural analyses pathogen-activated NLR oligomers (resistosomes) reveal how different subtypes converge various ways calcium (Ca 2+ ) signaling promote pathogen host cell death. Especially striking is identification nucleotide-based signals generated enzymatically toll-interleukin 1 receptor (TIR) domain NLRs. These small molecules part an emerging family TIR-produced cyclic noncyclic nucleotide steer cell-death responses bacteria, mammals, plants. A combined genetic, molecular, understanding activation provides exciting new opportunities combatting diseases [Formula: see text] Copyright © 2023 The Author(s). This open access article distributed under CC BY-NC-ND 4.0 International license .

Language: Английский

Citations

26
A disease resistance protein triggers oligomerization of its NLR helper into a hexameric resistosome to mediate innate immunity DOI Creative Commons
Jogi Madhuprakash, AmirAli Toghani, Mauricio P. Contreras

et al.

Science Advances, Journal Year: 2024, Volume and Issue: 10(45)

Published: Nov. 6, 2024

NRCs are essential helper NLR (nucleotide-binding domain and leucine-rich repeat) proteins that execute immune responses triggered by sensor NLRs. The resting state of NbNRC2 was recently shown to be a homodimer, but the sensor-activated remains unclear. Using cryo-EM, we determined structure NbNRC2, which forms hexameric inflammasome-like resistosome. Mutagenesis oligomerization interface abolished signaling, confirming functional significance Comparative structural analyses between homodimer homohexamer revealed substantial rearrangements, providing insights into activation mechanisms. Furthermore, comparisons hexamer previously reported CC-NLR pentameric assemblies features allowing an additional protomer integration. structure, assessed released AlphaFold 3 for predicting activated oligomers, revealing high-confidence modeling other amino-terminal α1 helices, region proven difficult resolve structurally. Overall, our work sheds light on mechanisms expands understanding diversity.

Language: Английский

Citations

10
The nucleotide‐binding domain of NRC‐dependent disease resistance proteins is sufficient to activate downstream helper NLR oligomerization and immune signaling DOI Creative Commons
Mauricio P. Contreras, Hsuan Pai, Rebecca Thompson

et al.

New Phytologist, Journal Year: 2024, Volume and Issue: 243(1), P. 345 - 361

Published: May 17, 2024

Summary Nucleotide‐binding domain and leucine‐rich repeat (NLR) proteins with pathogen sensor activities have evolved to initiate immune signaling by activating helper NLRs. However, the mechanisms underpinning NLR activation NLRs remain poorly understood. Although coiled coil (CC) type such as Potato virus X disease resistance protein Rx been shown activate oligomerization of their downstream helpers NRC2, NRC3 NRC4, domains involved in sensor–helper are not known. Here, we used Agrobacterium tumefaciens ‐mediated transient expression Nicotiana benthamiana show that nucleotide‐binding (NB) within NB‐ARC is necessary sufficient for In addition, NB Gpa2 (cyst nematode resistance), Rpi‐amr1, Rpi‐amr3 (oomycete resistance) Sw‐5b (virus also respective NRC helpers. Using lettuce ( Lactuca sativa ), (both full length or truncation) its NRC2 form a minimal functional unit can be transferred from solanaceous plants (lamiids) Campanulid species. Our results challenge prevailing paradigm exclusively signal via N‐terminal reveal activity NRC‐dependent We propose model which perceive status upstream sensors.

Language: Английский

Citations

9
A cell wall-associated kinase phosphorylates NLR immune receptor to negatively regulate resistosome formation DOI
Chenchen Zhong, Wenli Li, Xinyu Zhang

et al.

Nature Plants, Journal Year: 2025, Volume and Issue: unknown

Published: March 21, 2025

Language: Английский

Citations

1
Molecular engineering of plant immune receptors for tailored crop disease resistance DOI Creative Commons

Lila Cadiou,

Francois Brunisholz,

Stella Césari

et al.

Current Opinion in Plant Biology, Journal Year: 2023, Volume and Issue: 74, P. 102381 - 102381

Published: May 15, 2023

The specific recognition of pathogen effectors by intracellular nucleotide-binding and leucine-rich repeat domain receptors (NLRs) is an important component plant immunity. Creating NLRs with new bespoke specificities a major goal in molecular pathology as it promises to provide unlimited resources for the resistance crops against diseases. Recent breakthrough discoveries on structure activity begin enable their knowledge-guided engineering. First, studies succeeded extend or change effector modifying, structure-guided manner, NLR domains that directly bind effectors. By modifying LRR singleton Sr35 unconventional decoy helper RGA5 Pik-1, detected other additional were created.

Language: Английский

Citations

21