To survive in an ever-changing environment, plants must control their cellular ion homeostasis tightly. In this regard, Ca2+ signaling represents a central motif inherent to numerous pathways ...controlling this process
Abstract
Soil composition largely defines the living conditions of plants and represents one of their most relevant, dynamic, and complex environmental cues. The effective concentrations of many either tolerated or essential ions and compounds in the soil usually differ from the optimum that would be most suitable for plants. In this regard, salinity-caused by excess NaCl-represents a widespread adverse growth condition, but shortage of ions such as K+, NO3−, and Fe2+ also restrains plant growth. During the past years, many components and mechanisms that function in the sensing and establishment of ion homeostasis have been identified and characterized. Here, we reflect on recent insights that extended our understanding of components and mechanisms which govern and fine-tune plant salt stress tolerance and ion homeostasis. We put special emphasis on mechanisms that allow for interconnection of the salt overly sensitive pathway with plant development and discuss newly emerging functions of Ca2+ signaling in salinity tolerance. Moreover, we review and discuss accumulating evidence for a central and unifying role for Ca2+ signaling and Ca2+-dependent protein phosphorylation in regulating sensing, uptake, transport, and storage processes of various ions. Finally, based on this cross-field inventory, we deduce emerging concepts and questions arising for future research.
Deciphering signal transduction processes is crucial for understanding how plants sense and respond to environmental changes. Various chemical compounds function as central messengers within deeply ...intertwined signaling networks. How such compounds act in concert remains to be elucidated. We have developed dual-reporting transcriptionally linked genetically encoded fluorescent indicators (2-in-1-GEFIs) for multiparametric in vivo analyses of the phytohormone abscisic acid (ABA), Ca
, protons (H
), chloride (anions), the glutathione redox potential, and H
O
Simultaneous analyses of two signaling compounds in Arabidopsis (
) roots revealed that ABA treatment and uptake did not trigger rapid cytosolic Ca
or H
dynamics. Glutamate, ATP, Arabidopsis PLANT ELICITOR PEPTIDE, and glutathione disulfide (GSSG) treatments induced rapid spatiotemporally overlapping cytosolic Ca
, H
, and anion dynamics, but except for GSSG, only weakly affected the cytosolic redox state. Overall, 2-in-1-GEFIs enable complementary, high-resolution in vivo analyses of signaling compound dynamics and facilitate an advanced understanding of the spatiotemporal coordination of signal transduction processes in Arabidopsis.
• RBOHF from Arabidopsis thaliana represents a multifunctional NADPH oxidase regulating biotic and abiotic stress tolerance, developmental processes and guard cell aperture. The molecular components ...and mechanisms determining RBOHF activity remain to be elucidated.
• Here we combined protein interaction studies, biochemical and genetic approaches, and pathway reconstitution analyses to identify and characterize proteins that confer RBOHF regulation and elucidated mechanisms that adjust RBOHF activity.
• While the Ca2+ sensor-activated kinases CIPK11 and CIPK26 constitute alternative paths for RBOHF activation, the combined activity of CIPKs and the kinase open stomata 1 (OST1) triggers complementary activation of this NADPH oxidase, which is efficiently counteracted through dephosphorylation by the phosphatase ABI1. Within RBOHF, several distinct phosphorylation sites (p-sites) in the N-terminus of RBOHF appear to contribute individually to activity regulation.
• These findings identify RBOHF as a convergence point targeted by a complex regulatory network of kinases and phosphatases. We propose that this allows for fine-tuning of plant reactive oxygen species (ROS) production by RBOHF in response to different stimuli and in diverse physiological processes.
Guard cells integrate various hormone signals and environmental cues to balance plant gas exchange and transpiration. The wounding-associated hormone jasmonic acid (JA) and the drought hormone ...abscisic acid (ABA) both trigger stomatal closure. In contrast to ABA however, the molecular mechanisms of JA-induced stomatal closure have remained largely elusive. Here, we identify a fast signaling pathway for JA targeting the K+ efflux channel GORK. Wounding triggers both local and systemic stomatal closure by activation of the JA signaling cascade followed by GORK phosphorylation and activation through CBL1-CIPK5 Ca2+ sensor-kinase complexes. GORK activation strictly depends on plasma membrane targeting and Ca2+ binding of CBL1-CIPK5 complexes. Accordingly, in gork, cbl1, and cipk5 mutants, JA-induced stomatal closure is specifically abolished. The ABA-coreceptor ABI2 counteracts CBL1-CIPK5-dependent GORK activation. Hence, JA-induced Ca2+ signaling in response to biotic stress converges with the ABA-mediated drought stress pathway to facilitate GORK-mediated stomatal closure upon wounding.
•Wounding triggers stomatal closure by activating COI1-dependent guard cell jasmonate signaling•The guard cell K+ efflux channel GORK is required for jasmonate-induced stomatal closure•The Ca2+ sensor-kinase CBL1-CIPK5 complex phosphorylates and activates the GORK channel•Kinase channel activation is antagonized by ABI2, indicating jasmonate and ABA crosstalk
Plant stomata regulate gas exchange with the environment in response to various signals, including the wounding-associated hormone jasmonate. Förster et al. delineate the relevant signaling pathway downstream of jasmonate, modulating the activity of the K+ efflux channel GORK, and identify an interaction with abscisic acid (ABA) signaling.
Ca2+ signals are transient, hence, upon a stimulus-induced increase in cytosolic Ca2+ concentration, cells have to re-establish resting Ca2+ levels. Ca2+ extrusion is operated by a wealth of ...transporters, such as Ca2+ pumps and Ca2+/H⁺ antiporters, which often require a rise in Ca2+ concentration to be activated. Here, we report a regulatory fine-tuning mechanism of the Arabidopsis thaliana plasma membrane-localized Ca2+-ATPase isoform ACA8 that is mediated by calcineurin B-like protein (CBL) and CBL-interacting protein kinase (CIPK) complexes. We show that two CIPKs (CIPK9 and CIPK14) are able to interact with ACA8 in vivo and phosphorylate it in vitro. Transient co-overexpression of ACA8 with CIPK9 and the plasma membrane Ca2+ sensor CBL1 in tobacco leaf cells influences nuclear Ca2+ dynamics, specifically reducing the height of the second peak of the wound-induced Ca2+ transient. Stimulus-induced Ca2+ transients in mature leaves and seedlings of an aca8 T-DNA insertion line exhibit altered dynamics when compared with the wild type. Altogether our results identify ACA8 as a prominent in vivo regulator of cellular Ca2+ dynamics and reveal the existence of a Ca2+-dependent CBL–CIPK-mediated regulatory feedback mechanism, which crucially functions in the termination of Ca2+ signals.
N-myristoylation and S-acylation promote protein membrane association, allowing regulation of membrane proteins. However, how widespread this targeting mechanism is in plant signaling processes ...remains unknown.
Through bioinformatics analyses, we determined that among plant protein kinase families, the occurrence of motifs indicative for dual lipidation by N-myristoylation and S-acylation is restricted to only five kinase families, including the Ca2+-regulated CDPK-SnRK and CBL protein families. We demonstrated N-myristoylation of CDPK-SnRKs and CBLs by incorporation of radiolabeled myristic acid. We focused on CPK6 and CBL5 as model cases and examined the impact of dual lipidation on their function by fluorescence microscopy, electrophysiology and functional complementation of Arabidopsis mutants.
We found that both lipid modifications were required for proper targeting of CBL5 and CPK6 to the plasma membrane. Moreover, we identified CBL5–CIPK11 complexes as phosphorylating and activating the guard cell anion channel SLAC1. SLAC1 activation by CPK6 or CBL5–CIPK11 was strictly dependent on dual lipid modification, and loss of CPK6 lipid modification prevented functional complementation of cpk3 cpk6 guard cell mutant phenotypes.
Our findings establish the general importance of dual lipid modification for Ca2+ signaling processes, and demonstrate their requirement for guard cell anion channel regulation.
Root hairs (RH) are tip growing polarized cells aiding the uptake of nutrients and water into plants. RH differentiation involves the interplay of various hormones and second messengers. Tightly ...regulated production of reactive oxygen species by the NADPH oxidase RBOHC crucially functions in RH differentiation and Ca2+‐dependent phosphorylation has been implemented in these processes. However, the kinases regulating RBOHC remained enigmatic. Here we identify CBL1‐CIPK26 Ca2+ sensor‐kinase complexes as modulators of RBOHC activity. Combined genetic, cell biological and biochemical analyses reveal synergistic function of CIPK26‐mediated phosphorylation and Ca2+ binding for RBOHC activation. Complementation of rbohC mutant RH phenotypes by a S318/322 phosphorylation deficient RBOHC version suggests flexible and alternating phosphorylation patterns as mechanism fine‐tuning ROS production in RH development.
Ca2+ signals in plant immunity Köster, Philipp; DeFalco, Thomas A; Zipfel, Cyril
The EMBO journal,
14 June 2022, Letnik:
41, Številka:
12
Journal Article
Recenzirano
Odprti dostop
Calcium ions function as a key second messenger ion in eukaryotes. Spatially and temporally defined cytoplasmic Ca2+ signals are shaped through the concerted activity of ion channels, exchangers, and ...pumps in response to diverse stimuli; these signals are then decoded through the activity of Ca2+‐binding sensor proteins. In plants, Ca2+ signaling is central to both pattern‐ and effector‐triggered immunity, with the generation of characteristic cytoplasmic Ca2+ elevations in response to potential pathogens being common to both. However, despite their importance, and a long history of scientific interest, the transport proteins that shape Ca2+ signals and their integration remain poorly characterized. Here, we discuss recent work that has both shed light on and deepened the mysteries of Ca2+ signaling in plant immunity.
This review summarizes how calcium ions, and the proteins which transport them, are integrated into plant immune responses.
Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant ...protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of ArinaLrFor, an Lr14a-containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca
-permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a. Haplotype analyses indicate that Lr14a-containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding.
Austenitic–ferritic duplex steels are used for structural applications when high strength in combination with excellent corrosion resistance is required. Many of these applications imply cyclic ...loading and hence, fatigue damage needs to be considered for dimensioning. Most dimensioning strategies make use of the fatigue-limit concept. However, while the original fatigue-limit concept is based on the idea that existing slip bands or microcracks are blocked by microstructural barriers like grain or phase boundaries, more recent research work has shown that metallic structures may fail far below the conventional fatigue limit even at very high numbers of cycles to fracture. The present paper deals with the observation of local plasticity and fatigue damage in the VHCF regime by means of high-frequency fatigue testing in combination with scanning electron microscopy (SEM) and with electron back-scattered diffraction (EBSD). The results reveal that fatigue damage in the VHCF regime indeed causes the formation of slip bands followed by initiation and propagation of microstructurally short cracks in a very localized manner, manifesting itself by heat generation. The SEM observations and measurements of slip band geometries were correlated with calculations using a finite-element and a numerical short-crack model, which take the real two-phase microstructure and its elastic/plastic anisotropy into account and allow the prediction of both: (i) the fatigue crack initiation sites and (ii) microcrack propagation rates.
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