Plant nucleotide-binding leucine-rich repeat receptors (NLRs) regulate immunity and cell death. In
Calcium serves as a second messenger in a variety of developmental and physiological processes and has long been identified as important for plant immune responses. We discuss recent discoveries regarding plant immune‐related calcium‐permeable channels and how the two intertwined branches of the plant immune system are intricately linked to one another through calcium signalling. Cell surface immune receptors carefully tap the immense calcium gradient that exists between apoplast and cytoplasm in a short burst via tightly regulated plasma membrane (PM)‐resident cation channels. Intracellular immune receptors form atypical calcium‐permeable cation channels at the PM and mediate a prolonged calcium influx, overcoming the deleterious influence of pathogen effectors and enhancing plant immune responses.
more » « less- PAR ID:
- 10364613
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 234
- Issue:
- 3
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- p. 813-818
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Arabidopsis , a subfamily of “helper” NLRs is required by many “sensor” NLRs. Active NRG1.1 oligomerized, was enriched in plasma membrane puncta, and conferred cytoplasmic calcium ion (Ca2+) influx in plant and human cells. NRG1.1-dependent Ca2+influx and cell death were sensitive to Ca2+channel blockers and were suppressed by mutations affecting oligomerization or plasma membrane enrichment. Ca2+influx and cell death mediated by NRG1.1 and ACTIVATED DISEASE RESISTANCE 1 (ADR1), another helper NLR, required conserved negatively charged N-terminal residues. Whole-cell voltage-clamp recordings demonstrated thatArabidopsis helper NLRs form Ca2+-permeable cation channels to directly regulate cytoplasmic Ca2+levels and consequent cell death. Thus, helper NLRs transduce cell death signals directly. -
null (Ed.)At the host–pathogen interface, the protein composition of the plasma membrane (PM) has important implications for how a plant cell perceives and responds to invading microbial pathogens. A plant's ability to modulate its PM composition is critical for regulating the strength, duration, and integration of immune responses. One mechanism by which plant cells reprogram their cell surface is vesicular trafficking, including secretion and endocytosis. These trafficking processes add or remove cargo proteins (such as pattern-recognition receptors, transporters, and other proteins with immune functions) to or from the PM via small, membrane-bound vesicles. Clathrin-coated vesicles (CCVs) that form at the PM and trans-Golgi network/early endosomes have emerged as the prominent vesicle type in the regulation of plant immune responses. In this review, we discuss the roles of the CCV core, adaptors, and accessory components in plant defense signaling and immunity against various microbial pathogens.more » « less
-
more » « less
Iron- and reactive oxygen species (ROS)-dependent ferroptosis occurs in plant cells. Ca2+acts as a conserved key mediator to control plant immune responses. Here, we report a novel role of cytoplasmic Ca2+influx regulating ferroptotic cell death in rice immunity using pharmacological approaches. High Ca2+influx triggered iron-dependent ROS accumulation, lipid peroxidation, and subsequent hypersensitive response (HR) cell death in rice (
Oryza sativa ). DuringMagnaporthe oryzae infection, 14 different Ca2+influx regulators altered Ca2+, ROS and Fe2+accumulation,glutathione reductase (GR ) expression, glutathione (GSH) depletion and lipid peroxidation, leading to ferroptotic cell death in rice. High Ca2+levels inhibited the reduction of glutathione isulphide (GSSG) to GSHin vitro . Ca2+chelation by ethylene glycol-bis (2-aminoethylether)-N, N, N’, N’ -tetra-acetic acid (EGTA) suppressed apoplastic Ca2+influx in rice leaf sheaths during infection. Blocking apoplastic Ca2+influx into the cytoplasm by Ca2+chelation effectively suppressed Ca2+-mediated iron-dependent ROS accumulation and ferroptotic cell death. By contrast, acibenzolar-S -methyl (ASM), a plant defense activator, significantly enhanced Ca2+influx, as well as ROS and iron accumulation to trigger ferroptotic cell death in rice. The cytoplasmic Ca2+influx through calcium-permeable cation channels, including the putative resistosomes, could mediate iron- and ROS-dependent ferroptotic cell death under reducedGR expression levels in rice immune responses. -
more » « less
Intracellular plant immune receptors, termed NLRs (Nucleotide-binding Leucine-rich repeat Receptors), confer effector-triggered immunity. Sensor NLRs are responsible for pathogen effector recognition. Helper NLRs function downstream of sensor NLRs to transduce signaling and induce cell death and immunity. Activation of sensor NLRs that contain TIR (Toll/interleukin-1receptor) domains generates small molecules that induce an association between a downstream heterodimer signalosome of EDS1 (EnhancedDisease Susceptibility 1)/SAG101 (Senescence-AssociatedGene 101) and the helper NLR of NRG1 (NRequired Gene 1). Autoactive NRG1s oligomerize and form calcium signaling channels largely localized at the plasma membrane (PM). The molecular mechanisms of helper NLR PM association and effector-induced NRG1 oligomerization are not well characterized. We demonstrate that helper NLRs require positively charged residues in their N-terminal domains for phospholipid binding and PM association before and after activation, despite oligomerization and conformational changes that accompany activation. We demonstrate that effector activation of a TIR-containing sensor NLR induces NRG1 oligomerization at the PM and that the cytoplasmic pool of EDS1/SAG101 is critical for cell death function. EDS1/SAG101 cannot be detected in the oligomerized NRG1 resistosome, suggesting that additional unknown triggers might be required to induce the dissociation of EDS1/SAG101 from the previously described NRG1/EDS1/SAG101 heterotrimer before subsequent NRG1 oligomerization. Alternatively, the conformational changes resulting from NRG1 oligomerization abrogate the interface for EDS1/SAG101 association. Our data provide observations regarding dynamic PM association during helper NLR activation and underpin an updated model for effector-induced NRG1 resistosome formation.
-
more » « less
Abstract Waterlogging stress (WLS) negatively impacts the growth and yield of crops resulting in heavy losses to agricultural production. Previous studies have revealed that WLS induces a systemic response in shoots that is partially dependent on the plant hormones ethylene and abscisic acid. However, the role of rapid cell-to-cell signaling pathways, such as the reactive oxygen species (ROS) and calcium waves, in systemic responses of plants to WLS is unknown at present. Here, we reveal that an abrupt WLS treatment of Arabidopsis (Arabidopsis thaliana) plants growing in peat moss triggers systemic ROS and calcium wave responses and that the WLS-triggered ROS wave response of Arabidopsis is dependent on the ROS-generating RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD), calcium-permeable channels GLUTAMATE-LIKE RECEPTOR 3.3 and 3.6 (GLR3.3 and GLR3.6), and aquaporin PLASMA MEMBRANE INTRINSIC PROTEIN 2;1 (PIP2;1) proteins. We further show that WLS is accompanied by a rapid systemic transcriptomic response that is evident as early as 10 min following waterlogging initiation, includes many hypoxia-response transcripts, and is partially dependent on RBOHD. Interestingly, the abrupt WLS of Arabidopsis resulted in the triggering of a rapid hydraulic wave response and the transient opening of stomata on leaves. In addition, it induced in plants a heightened state of tolerance to a subsequent submergence stress. Taken together, our findings reveal that the initiation of WLS in plants is accompanied by rapid systemic physiological and transcriptomic responses that involve the ROS, calcium, and hydraulic waves, as well as the induction of hypoxia acclimation mechanisms in systemic tissues.
