Calcium: silver bullet in signaling

Plant molecular biology, 1998

In the plants being exposed to environmental stresses, ion channels are likely activated to convert these external stimuli into intracellular signals. Among the ions taken up by the plant cells, Ca2+ plays an essential role as an intracellular secondary messenger in plants and thus the cytoplasmic free Ca2+ concentration ([Ca2+]c) is strictly regulated. Signal transduction pathways mediated by the changes in the [Ca2+]c is termed Ca2+ signaling, and are mainly initiated by the activation of Ca2+-permeable channels. When Ca2+ channels are activated in response to a variety stimuli, a drastic increase in the [Ca2+]c is induced and the entered free Ca2+ binds to the sets of Ca2+-regulated proteins such as calmodulin and calcium dependent protein kinases to modify the activities or affinities of these proteins in binding to specific targets. To date, a large body of electro-physiological and molecular biological studies has revealed that plants possess several Ca2+ channels belonging to distinct types with different gating mechanisms, and a variety of genes for Ca2+-permeable channels have been isolated and functionally characterized. In this chapter, the topics covered include (1) the characteristics of molecularly cloned Ca2+-permeable channels including voltage-dependent Ca2+-permeable channels, cyclic nucleotide-gated cation channel, and ionotropic glutamate receptor; (2) the roles of Ca2+ at the key steps during environmental responses and regulations of growth and developments (eg. stomatal movements, tropisms, nutrient allocations, flowering, pollination, fertilization, and etc.); (3) the Ca2+-dependent metabolic regulation of reactive oxygen species levels; and (4) the Ca2+-mediated response during plant defense mechanism against pathogenic microorganisms.

Journal of experimental botany, 2018

Calcium (Ca2+) is among the most important intracellular messengers in living organisms. Understanding of the players and dynamics of Ca2+ signalling pathways in plants may help to unravel the molecular basis of their exceptional flexibility to respond and to adapt to different stimuli. In the present review we focus on new tools that have recently revolutionized our view of organellar Ca2+ signalling as well as on the current knowledge regarding the pathways mediating Ca2+ fluxes across intracellular membranes. The contribution of organelles and cellular subcompartments to the orchestrated response via Ca2+ signalling within a cell is also discussed, underlining the fact that one of the greatest challenges in the field is the elucidation of how influx and efflux Ca2+ transporters/channels are regulated in a concerted manner to translate specific information into a Ca2+ signature.

Ca2+ signals are involved in most aspects of growth and development of plant, including response to hormone signaling, various biotic and abiotic stresses, germination, cell division, cell expansion, pollen tube growth and fertilization. The calcium-dependent protein kinases (CDPKs) constitute one of the largest Ca 2+ sensing subfamilies of plant-specific protein kinases that decodes the transient changes of Ca 2+ concentration in the cytoplasm in response to extrinsic and intrinsic cues. The unique domain structure of CDPKs makes them not only " sensors " but also " responders " to these Ca 2+ signatures. A multigene family consisting of 34, 31 and 20 genes in Arabidopsis, rice and wheat, respectively, encodes CDPKs. The multigenic nature and diverse spatial and temporal differential expression have been reported in many plant species, which emphasizes on the precise role of isoforms in developmental (e.g. pollen tube) as well as stress responsive pathways (e.g. ROS). The regulation of CDPKs has been reported to be at transcriptional and post translational level. The signaling pathways mediated by CDPKs have also been found to overlap with MAP kinase pathways, suggesting of an intricate network, which regulate precise responses of plants. The proteins interacting with CDPKs are diverse in their function (e.g. transcription factor, channel protein, v-SNARE) which indicates that CDPKs play important role in regulating the Ca 2+ signaling cascade, leading to extremely precise response of plants during development and adaptation to environmental cues. This functional diversity and their cross-talks are being discussed in this review.

International Journal of Molecular Sciences, 2018

Among the most recently discovered chemical regulators of plant growth and development are extracellular nucleotides, especially extracellular ATP (eATP) and extracellular ADP (eADP). Plant cells release ATP into their extracellular matrix under a variety of different circumstances, and this eATP can then function as an agonist that binds to a specific receptor and induces signaling changes, the earliest of which is an increase in the concentration of cytosolic calcium ([Ca2+]cyt). This initial change is then amplified into downstream-signaling changes that include increased levels of reactive oxygen species and nitric oxide, which ultimately lead to major changes in the growth rate, defense responses, and leaf stomatal apertures of plants. This review presents and discusses the evidence that links receptor activation to increased [Ca2+]cyt and, ultimately, to growth and diverse adaptive changes in plant development. It also discusses the evidence that increased [Ca2+]cyt also enhan...

Physiology and Molecular Biology of Plants, 2008

In the environment, plants are exposed to plethora of adverse stimuli such as abiotic and biotic stresses. Abiotic stresses including dehydration, salinity and low temperature poses a major threat for crop productivity. Plant responds to these stresses by activating a number of signaling pathways which enable them to defend or adjust against these stresses. To understand the mechanisms by which plants perceive environmental signals and transmit these signals to cellular machinery to activate adaptive responses is of fundamental importance to biology. Calcium plays a pivotal role in plant responses to a number of stimuli including pathogens, abiotic stresses, and hormones. However, the molecular mechanisms underlying calcium functions are poorly understood. It is hypothesized that calcium serves as second messenger and, in many cases, requires intracellular protein sensors to transduce the signal further downstream in the pathways. Recently a novel calcium signaling pathway which consist of calcineurin B-like protein (CBL) calcium sensor and CBL-interacting protein kinase (CIPK) network as a newly emerging signaling system mediating a complex array of environmental stimuli. This review focuses on the overview of functional aspects of CBL and CIPK in plants. In addition, an attempt has also been made to categorize the functions of this CBL-CIPK pair in major signaling pathways in plants.

Molecular Plant, 2010

The past two decades revealed a plethora of Ca 21-responsive proteins and downstream targets in plants, of which several are unique to plants. More recent high-throughput 'omics' approaches and bioinformatics are exposing Ca 21-responsive cis-elements and the corresponding Ca 21-responsive genes. Here, we review the current knowledge on Ca 21-signaling pathways that regulate gene expression in plants, and we link these to mechanisms by which plants respond to biotic and abiotic stresses.

Critical Reviews in Plant Sciences, 2017

Calcium-dependent protein kinases (CDPKs) form the major and unique group of calcium (Ca 2C) sensors in plants. Attributed to their peculiar structural features, CDPKs play a dual role of "Ca 2C sensor and responder" and translate the message from specific Ca 2C signature to phosphorylation events. Most of the stress and developmental triggers instigate an increase in Ca 2C level and consequently Ca 2C signaling in plants. Expression and functional analyses across plant species have revealed differential regulation of CDPK transcripts, activity, protein interactions and substrate targeting under different cues, including biotic and abiotic stresses and plant development. Thus, vital roles of CDPKs are proposed in perpetuating stress and development triggered Ca 2C signaling to adaptive responses in plants. Genetic engineering using CDPK genes could be utilitarian in the agricultural biotechnology for imparting higher degree of biotic and abiotic stress tolerance and better productivity. Here, we discuss the recent advancements and update of CDPK gene family organization, domain structure and regulatory mechanism, the role of CDPKs in abiotic stress, biotic stress, development signaling and responses in the model and crop plants.

In response to any stimulus, various cellular responses are triggered among, which the most rapid responses include the induction of calcium and reactive oxygen species (ROS) transients. The induction of calcium transient is due to the concerted action of calcium dependent channels, pumps, and carriers situated in the plasma membrane and different sub-cellular compartments. The spatial and temporal nature of the calcium transient is defined as cellular " Ca 2+ signature " and is responsible for the activation of stimulus-specific calcium sensor and decoder elements. The redox state of the cell under any condition is defined as the integrative ratio of reduced to oxidized form of redox couples present inside the cell. The induction of calcium transient is coherent with the significantly higher level of ROS, which shifts the redox status of the cell to a more oxidized state. This change occurs in a dose dependent manner and is sensed in calcium signaling dependent manner. The complex and coordinated interaction of calcium and redox events is responsible for the generation of stimulus-specific response. The present article deals with the overview of calcium and redox signaling events and their possible crosstalk to regulate different plant functions under normal and stressful environment.

2014

The calcium ion (Ca 2+ ) is a versatile intracellular messenger. It provides dynamic regulation of a vast array of gene transcriptions, protein kinases, transcription factors and other complex downstream signaling cascades. For the past six decades, intracellular Ca 2+ concentration has been significantly studied and still many studies are under way. Our understanding of Ca 2+ signaling and the corresponding physiological phenomenon is growing exponentially. Here we focus on the improvements made in the development of probes used for Ca 2+ imaging and expanding the application of Ca 2+ imaging in plant science research.

International Journal of Current Microbiology and Applied Sciences, 2020

Calcium is an essential macro-nutrient in plants, with concentrations in the shoot ranging from 0.1 to 5% of dry wt.Ca 2+ is taken up by the root and transported to the shoot in a mainly apoplastic way to avoid interference with its function as second messenger. To circumvent the casparian strip, it has to enter the cytosol of the endodermal cells via channel proteins and subsequently be exported into the apoplast via Ca 2+-ATPases or Ca 2+ /H + anti porters. H + /Ca 2+ anti porters and Ca 2+-ATPases, which actively deliver Ca 2+ into the apoplast or intracellular stores. These channels maintain a low (Ca 2+) cyt in the resting (un-stimulated) cell appropriate for Cytoplasmic metabolism,restore (Ca 2+) cyt to resting levels following a (Ca 2+) cyt perturbation (stimulated). Ca 2+ contributes to the structure of cell wall, stability of cell membrane, photosynthetic reaction, photo-protection (D1 protein, PsbS regulated by Ca 2+), stomatal movement and pollen tube growth and elongation. Calcium sensors, including calmodulin (CaM), calmodulin-like (CML) proteins, calcineurin B-like proteins (CBL), and calcium-dependent protein kinases (CDPK) helps in Ca 2+ signaling pathway during stress and non-stress condition. Deficiency symptoms occur more often in developing tissue such as young leaves and fruits, due to low remobilization from old to young tissue via the phloem. This leads to a strong dependency of Ca 2+ supply via the xylem. Resulting physiological disorder are tip burn in lettuce or blossom end rot in tomato. Plants deficient in calcium have been shown to be more susceptible to pathogens and exogenous calcium supply in turn has been shown to improve the plant's resistance. Conserved microbial patterns for example PAMP initiating a signaling cascade leading to induction of downstream responses of defense gene expression. Future research will shed more light on the different functions of this important nutrient and how they are interconnected.

Molecular Plant, 2012

Calcium acts as a second messenger for signaling to a variety of stimuli including MAMPs (Microbe-Associated Molecular Patterns), such as flg22 and elf18 that are derived from bacterial flagellin and elongation factor Tu, respectively. Here, Arabidopsis thaliana mutants with changed calcium elevation (cce) in response to flg22 treatment were isolated and characterized. Besides novel mutant alleles of the flg22 receptor, FLS2 (Flagellin-Sensitive 2), and the receptor-associated kinase, BAK1 (Brassinosteroid receptor 1-Associated Kinase 1), the new cce mutants can be categorized into two main groups-those with a reduced or an enhanced calcium elevation. Moreover, cce mutants from both groups show differential phenotypes to different sets of MAMPs. Thus, these mutants will facilitate the discovery of novel components in early MAMP signaling and bridge the gaps in current knowledge of calcium signaling during plant-microbe interactions. Last but not least, the screening method is optimized for speed (covering 384 plants in 3 or 10 h) and can be adapted to genetically dissect any other stimuli that induce a change in calcium levels.

Cold Spring Harbor Protocols, 2013

Temporally and spatially defined changes in cellular calcium (Ca(2+)) concentration represent stimulus-specific signals and regulate a myriad of biological processes. The development of ratiometric Ca(2+) reporter proteins like Yellow Cameleons (YCs) has greatly advanced our ability to analyze Ca(2+) dynamics in vivo with unprecedented spatial and temporal resolution. In plants, the application of these Ca(2+) reporter proteins has been pioneered for the investigation of Ca(2+) dynamics in guard cells, and recently their use has been extended to other single-cell models like growing pollen tubes and root hairs. However, in plants, the use of YC reporter proteins has largely remained restricted to the investigation of cytoplasmic alterations of Ca(2+) concentrations. Here, we provide an introduction to current methods for imaging Ca(2+) dynamics with increasing sophistication.

PLANT PHYSIOLOGY, 2012

Plasma membrane-resident receptor kinases (RKs) initiate signaling pathways important for plant immunity and development. In Arabidopsis (Arabidopsis thaliana), the receptor for the elicitor-active peptide epitope of bacterial flagellin, flg22, is encoded by FLAGELLIN SENSING2 (FLS2), which promotes plant immunity. Despite its relevance, the molecular components regulating FLS2mediated signaling remain largely unknown. We show that plasma membrane ARABIDOPSIS-AUTOINHIBITED Ca 2+ -ATPase (ACA8) forms a complex with FLS2 in planta. ACA8 and its closest homolog ACA10 are required for limiting the growth of virulent bacteria. One of the earliest flg22 responses is the transient increase of cytosolic Ca 2+ ions, which is crucial for many of the well-described downstream responses (e.g. generation of reactive oxygen species and the transcriptional activation of defense-associated genes). Mutant aca8 aca10 plants show decreased flg22-induced Ca 2+ and reactive oxygen species bursts and exhibit altered transcriptional reprogramming. In particular, mitogen-activated protein kinase-dependent flg22-induced gene expression is elevated, whereas calcium-dependent protein kinase-dependent flg22-induced gene expression is reduced. These results demonstrate that the fine regulation of Ca 2+ fluxes across the plasma membrane is critical for the coordination of the downstream microbe-associated molecular pattern responses and suggest a mechanistic link between the FLS2 receptor complex and signaling kinases via the secondary messenger Ca 2+ . ACA8 also interacts with other RKs such as BRI1 and CLV1 known to regulate plant development, and both aca8 and aca10 mutants show morphological phenotypes, suggesting additional roles for ACA8 and ACA10 in developmental processes. Thus, Ca 2+ ATPases appear to represent general regulatory components of RK-mediated signaling pathways.

HortScience

In recent years evidence has been presented that implicates the role of free (cytosolic) Ca2+ as a major metabolic and developmental controller in plants. Calcium concentrations in the cytoplasm are kept very low under normal conditions (10-6 to 10-8 M). Small changes in the absolute amount of calcium can create a 10- to 100-fold change in the Ca2+ concentration without upsetting the ionic balance of the ceil. This feature makes Ca2+ an excellent candidate as a second messenger. Thus, a stress induced change in the cytosolic Ca2+ could bring a cellular/plant response to stress. This response is thought to be mediated through activation of Ca2+ and/or Ca2+-calmodulin-dependent protein kinases which in turn mediate the activity of various enzymes via phosphorylation. Recent evidences from the impact of salinity, low temperature, high temperature, and biotic stresses support such a role of calcium. Data on the association between stress-induced injury and perturbation of membrane/cytos...