Time-resolved single-cell and spatial gene regulatory atlas of plants under pathogen attack DOI Creative Commons
Tatsuya Nobori, Alexander Monell, Travis Lee

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: April 10, 2023

Abstract Plant leaf intercellular space provides a nutrient-rich and heterogeneous niche for microbes that critically impacts plant health. However, how individual cells respond to microbial colonization remains largely elusive. Here, by time-resolved simultaneous single-cell transcriptome epigenome profiling of plants ( Arabidopsis thaliana ) infected virulent avirulent bacterial pathogens Pseudomonas syringae ), we present cell atlases with gene regulatory logic involving transcription factors, putative cis -regulatory elements, target genes associated disease immunity. We also identify previously uncharacterized populations distinct immune expression within major developmental types. Furthermore, employ spatial transcriptomics reveal heterogeneity responses linked pathogen distribution. Integrating our multiomics omics data enables spatiotemporal mapping defense cells. Our study molecularly-defined map plant-microbe interaction at the resolution.

Language: Английский

Shared TIR enzymatic functions regulate cell death and immunity across the tree of life DOI
Kow Essuman, Jeffrey Milbrandt, Jeffery L. Dangl

et al.

Science, Journal Year: 2022, Volume and Issue: 377(6605)

Published: July 7, 2022

In the 20th century, researchers studying animal and plant signaling pathways discovered a protein domain that is shared across diverse innate immune systems: Toll/interleukin-1/resistance gene (TIR) domain. The TIR found in several architectures was defined as an adaptor mediates protein-protein interactions immunity developmental pathways. However, studies of nerve degeneration animals-and subsequent breakthroughs plant, bacterial, archaeal systems-revealed domains possess enzymatic activities. We provide synthesis functions role various related products evolutionarily systems. These may ultimately guide interventions would span tree life, from treating human neurodegenerative disorders bacterial infections to preventing diseases.

Language: Английский

Citations

101
The plant immune system: From discovery to deployment DOI Creative Commons
Jonathan D. G. Jones, Brian J. Staskawicz, Jeffery L. Dangl

et al.

Cell, Journal Year: 2024, Volume and Issue: 187(9), P. 2095 - 2116

Published: April 1, 2024

Plant diseases cause famines, drive human migration, and present challenges to agricultural sustainability as pathogen ranges shift under climate change. breeders discovered Mendelian genetic loci conferring disease resistance specific isolates over 100 years ago. Subsequent breeding for underpins modern agriculture and, along with the emergence focus on model plants genetics genomics research, has provided rich resources molecular biological exploration last 50 years. These studies led identification of extracellular intracellular receptors that convert recognition microbe-encoded patterns or pathogen-delivered virulence effectors into defense activation. receptor systems, downstream responses, define plant immune systems have evolved since migration land ∼500 million Our current understanding provides platform development rational enhancement control many continue plague crop production.

Language: Английский

Citations

93
Pathogen effector AvrSr35 triggers Sr35 resistosome assembly via a direct recognition mechanism DOI Creative Commons
Yan‐Bo Zhao, Mengxi Liu, Tao-Tao Chen

et al.

Science Advances, Journal Year: 2022, Volume and Issue: 8(36)

Published: Sept. 9, 2022

Nucleotide-binding, leucine-rich repeat receptors (NLRs) perceive pathogen effectors to trigger plant immunity. The direct recognition mechanism of by coiled-coil NLRs (CNLs) remains unclear. We demonstrate that the Triticum monococcum CNL Sr35 directly recognizes effector AvrSr35 from Puccinia graminis f. sp . tritici and report a cryo–electron microscopy structure resistosome crystal AvrSr35. show forms homodimers are disassociated into monomers upon domain Sr35, which induces assembly subsequent immune response. first 20 amino-terminal residues indispensable for signaling but not plasma membrane association. Our findings reveal activation provide insights biochemical function resistosome.

Language: Английский

Citations

82
Structural basis of NLR activation and innate immune signalling in plants DOI Creative Commons
Natsumi Maruta, Hayden Burdett, Bryan Y. J. Lim

et al.

Immunogenetics, Journal Year: 2022, Volume and Issue: 74(1), P. 5 - 26

Published: Jan. 4, 2022

Abstract Animals and plants have NLRs (nucleotide-binding leucine-rich repeat receptors) that recognize the presence of pathogens initiate innate immune responses. In plants, there are three types distinguished by their N-terminal domain: CC (coiled-coil) domain NLRs, TIR (Toll/interleukin-1 receptor) RPW8 (resistance to powdery mildew 8)-like coiled-coil NLRs. CC-NLRs (CNLs) TIR-NLRs (TNLs) generally act as sensors effectors secreted pathogens, while RPW8-NLRs (RNLs) signal downstream many sensor called helper Recent studies revealed dimensional structures a CNL (ZAR1) including its inactive, intermediate active oligomeric state, well TNLs (RPP1 ROQ1) in states. Furthermore, accumulating evidence suggests members family lipase-like EDS1 (enhanced disease susceptibility 1) proteins, which uniquely found seed play key role providing link between during Here, we summarize implications plant NLR provide insights into distinct mechanisms action different discuss NLR-mediated signalling pathways involving proteins RNLs.

Language: Английский

Citations

76
Molecular innovations in plant TIR-based immunity signaling DOI Creative Commons
Dmitry Lapin, Oliver Johanndrees, Zhongshou Wu

et al.

The Plant Cell, Journal Year: 2022, Volume and Issue: 34(5), P. 1479 - 1496

Published: Feb. 4, 2022

Abstract A protein domain (Toll and Interleukin-1 receptor [TIR]-like) with homology to animal TIRs mediates immune signaling in prokaryotes eukaryotes. Here, we present an overview of TIR evolution the molecular versatility domains different architectures for host protection against microbial attack. Plant TIR-based emerges as being central potentiation effectiveness defenses triggered by intracellular cell-surface receptors. Equally relevant plant fitness are mechanisms that limit potent healthy tissues but maintain preparedness infection. We propose seed plants evolved a specialized module selectively translate enzymatic activities defense outputs, overlaying more general function TIRs.

Language: Английский

Citations

76
A tale of many families: calcium channels in plant immunity DOI Open Access
Guangyuan Xu, Wolfgang Moeder, Keiko Yoshioka

et al.

The Plant Cell, Journal Year: 2022, Volume and Issue: 34(5), P. 1551 - 1567

Published: Jan. 28, 2022

Plants launch a concerted immune response to dampen potential infections upon sensing microbial pathogen and insect invasions. The transient rapid elevation of the cytosolic calcium concentration [Ca2+]cyt is among essential early cellular responses in plant immunity. free Ca2+ apoplast far higher than that resting cytoplasm. Thus, precise regulation channel activities infection key for an immediate dynamic influx trigger downstream signaling. Specific signatures different branches system vary timing, amplitude, duration, kinetics, sources Ca2+. Recent breakthroughs studies diverse groups classical channels highlight instrumental role homeostasis immunity cell survival. Additionally, identification some receptors as noncanonical Ca2+-permeable opens new view how initiate death This review aims provide overview Ca2+-conducting their molecular genetic mode-of-actions facilitating We also discuss regulatory mechanisms control stability activity these channels.

Language: Английский

Citations

72
Effector‐dependent activation and oligomerization of plant NRC class helper NLRs by sensor NLR immune receptors Rpi‐amr3 and Rpi‐amr1 DOI Creative Commons
Heekyung Ahn, Xiao Lin, Andrea Olave-Achury

et al.

The EMBO Journal, Journal Year: 2023, Volume and Issue: 42(5)

Published: Jan. 2, 2023

Abstract Plant pathogens compromise crop yields. Plants have evolved robust innate immunity that depends in part on intracellular Nucleotide‐binding, Leucine rich‐Repeat (NLR) immune receptors activate defense responses upon detection of pathogen‐derived effectors. Most “sensor” NLRs detect effectors require the activity “helper” NLRs, but how helper support sensor NLR function is poorly understood. Many Solanaceae NRC (NLR‐Required for Cell death) class NLRs. We show here Rpi‐amr3, a from Solanum americanum , detects AVRamr3 potato late blight pathogen, Phytophthora infestans and activates oligomerization NRC2 NRC4 into high‐molecular‐weight resistosomes. In contrast, recognition P. effector AVRamr1 by another Rpi‐amr1 induces formation only resistosome. The activated oligomer becomes enriched membrane fractions. ATP‐binding motifs both Rpi‐amr3 are required resistosome formation, not interaction with its cognate effector. can be homologs other species. Mechanistic understanding will underpin engineering crops durable disease resistance.

Language: Английский

Citations

64
NLR receptors in plant immunity: making sense of the alphabet soup DOI Creative Commons
Mauricio P. Contreras, Daniel Lüdke, Hsuan Pai

et al.

EMBO Reports, Journal Year: 2023, Volume and Issue: 24(10)

Published: Aug. 21, 2023

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

Language: Английский

Citations

60
Oligomerization of a plant helper NLR requires cell-surface and intracellular immune receptor activation DOI Creative Commons

Joanna M. Feehan,

Junli Wang, Xinhua Sun

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(11)

Published: March 6, 2023

Plant disease resistance involves both detection of microbial molecular patterns by cell-surface pattern recognition receptors and pathogen effectors intracellular NLR immune receptors. NLRs are classified as sensor NLRs, involved in effector detection, or helper required for signaling. TIR-domain-containing (TNLs) require NRG1 ADR1 resistance, activation defense requires the lipase-domain proteins EDS1, SAG101, PAD4. Previously, we found that associates with EDS1 SAG101 a TNL activation-dependent manner [X. Sun et al. , Nat. Commun. 12 3335 (2021)]. We report here how itself during TNL-initiated immunity. Full immunity coactivation mutual potentiation receptor-initiated signaling [B. P. M. Ngou, H.-K. Ahn, Ding, J. D. G. Jones, Nature 592 110–115 (2021), Yuan 105–109 find while TNLs is sufficient to promote NRG1–EDS1–SAG101 interaction, formation an oligomeric resistosome additional defense. These data suggest vivo part mechanism links receptor pathways.

Language: Английский

Citations

56
PTI‐ETI synergistic signal mechanisms in plant immunity DOI Creative Commons
Xiaoqian Yu,

Hao‐Qiang Niu,

Chao Liu

et al.

Plant Biotechnology Journal, Journal Year: 2024, Volume and Issue: 22(8), P. 2113 - 2128

Published: March 12, 2024

Summary Plants face a relentless onslaught from diverse array of pathogens in their natural environment, to which they have evolved myriad strategies that unfold across various temporal scales. Cell surface pattern recognition receptors (PRRs) detect conserved elicitors or endogenous molecules released during pathogen invasion, initiating the first line defence plants, known as pattern‐triggered immunity (PTI), imparts baseline level disease resistance. Inside host cells, effectors are sensed by nucleotide‐binding/leucine‐rich repeat (NLR) receptors, then activate second defence: effector‐triggered (ETI), offering more potent and enduring mechanism. Moreover, PTI ETI collaborate synergistically bolster resistance collectively trigger cascade downstream responses. This article provides comprehensive review plant responses, an overview stepwise activation interactions between PTI‐ETI synergistic signal transduction.

Language: Английский

Citations

48