The contribution of organelles to plant intracellular calcium signalling

Costa, Alex; Navazio, Lorella; Szabó, Ildikò

doi:10.1093/jxb/ery185

Cited by 108 publications

(121 citation statements)

References 241 publications

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“…As the Ca 2+ concentration of water is in the millimolar range, which is above the equilibrium dissociation constant of various forms of ATP to Ca 2+ and would therefore be toxic to the cell, cells have evolved ways to decrease the Ca 2+ concentration using pumps, transporters, and buffers. Cells typically maintain cytosolic free Ca 2+ concentrations at resting levels of ;50-200 nM, resulting in a substantial chemical Ca 2+ gradient among the cytosol, the extracellular space, and intracellular compartments (e.g., vacuole and endoplasmic reticulum) (Stael et al, 2012;Costa et al, 2018). Besides, the net electrical potentials existing across the plasma membrane (PM) and tonoplast contribute to building up large electrochemical gradients to drive for Ca 2+ transport.…”

Section: Introductionmentioning

confidence: 99%

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

et al. 2018

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Ca 2+ play a key role in cell signaling across organisms. The question of how a simple ion can mediate specific outcomes has spurred research into the role of Ca 2+ signatures and their encoding and decoding machinery. Such studies have frequently focused on Ca 2+ alone and our understanding of how Ca 2+ signaling is integrated with other responses is poor. Using in vivo imaging with different genetically encoded fluorescent sensors in Arabidopsis (Arabidopsis thaliana) cells, we show that Ca 2+ transients do not occur in isolation but are accompanied by pH changes in the cytosol. We estimate the degree of cytosolic acidification at up to 0.25 pH units in response to external ATP in seedling root tips. We validated this pH-Ca 2+ link for distinct stimuli. Our data suggest that the association with pH may be a general feature of Ca 2+ transients that depends on the transient characteristics and the intracellular compartment. These findings suggest a fundamental link between Ca 2+ and pH dynamics in plant cells, generalizing previous observations of their association in growing pollen tubes and root hairs. Ca 2+ signatures act in concert with pH signatures, possibly providing an additional layer of cellular signal transduction to tailor signal specificity.

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Section: Introductionmentioning

confidence: 99%

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

et al. 2018

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“…A complex Ca 2+ homeostatic and signaling machinery allows for a tight regulation of the intracellular concentration of the ion ([Ca 2+ ]) and its variations during signal transduction (Kudla et al, 2018). Plant organellar Ca 2+ signaling is a rapidly expanding field of investigation, also thanks to the increasing availability of novel genetically encoded Ca 2+ indicators, specifically targeted to different intracellular compartments (Costa et al, 2018). In addition to the vacuole, considered as the main stimulus-releasable Ca 2+ store in the plant cell, other organelles, i.e.…”

Section: Introductionmentioning

confidence: 99%

Chloroplast Calcium Signaling in the Spotlight

et al. 2020

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Calcium has long been known to regulate the metabolism of chloroplasts, concerning both light and carbon reactions of photosynthesis, as well as additional non photosynthesis-related processes. In addition to undergo Ca 2+ regulation, chloroplasts can also influence the overall Ca 2+ signaling pathways of the plant cell. Compelling evidence indicate that chloroplasts can generate specific stromal Ca 2+ signals and contribute to the fine tuning of cytoplasmic Ca 2+ signaling in response to different environmental stimuli. The recent set up of a toolkit of genetically encoded Ca 2+ indicators, targeted to different chloroplast subcompartments (envelope, stroma, thylakoids) has helped to unravel the participation of chloroplasts in intracellular Ca 2+ handling in resting conditions and during signal transduction. Intra-chloroplast Ca 2+ signals have been demonstrated to occur in response to specific environmental stimuli, suggesting a role for these plant-unique organelles in transducing Ca 2+ -mediated stress signals. In this mini-review we present current knowledge of stimulus-specific intrachloroplast Ca 2+ transients, as well as recent advances in the identification and characterization of Ca 2+ -permeable channels/transporters localized at chloroplast membranes. In particular, the potential role played by cMCU, a chloroplast-localized member of the mitochondrial calcium uniporter (MCU) family, as component of plant environmental sensing is discussed in detail, taking into account some specific structural features of cMCU. In summary, the recent molecular identification of some players of chloroplast Ca 2+ signaling has opened new avenues in this rapidly developing field and will hopefully allow a deeper understanding of the role of chloroplasts in shaping physiological responses in plants.

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“…The role of the Golgi as an important Ca 2+ store that contributes to Ca 2+ signaling in animal cells is established (Pizzo et al ., 2011). Although information on Ca 2+ handling by the plant Golgi is scarce (Costa et al ., 2018), it has been shown that free Ca 2+ concentration is higher in the Golgi than in the cytosol of plant cells, and abiotic cues can affect luminal Ca 2+ dynamics (Ordenes et al ., 2012). The nature and identity of Ca 2+ channels and transporters of the plant Golgi awaits clarification, although a role for P2A-type ATPase AtECA3 in the transport of Ca 2+ and Mn 2+ into the Golgi has been proposed (Mills et al ., 2008).…”

Section: Discussionmentioning

confidence: 99%

“…AtGAAP2/3/5, but not AtGAAP1/4, also localized in the tonoplast (Figure 5). The vacuole is the main storage compartment of Ca 2+ in plant cells (Peiter, 2011; Costa et al ., 2018) and many tonoplast Ca 2+ transporters have been identified (Martinoia et al ., 2012; Neuhaus and Trentmann, 2014; Costa et al ., 2018). Ca 2+ release from the vacuole likely contributes to signaling in plants and here evidence for a role for TPC1 as a tonoplast channel critical for many physiological processes is accumulating (Peiter et al ., 2005; Carpaneto and Gradogna, 2018).…”

Section: Discussionmentioning

confidence: 99%

Golgi anti-apoptotic proteins are evolutionarily conserved ion channels that regulate cell death in plants

Sierla

Prole

Saraiva

et al. 2019

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Programmed cell death regulates developmental and stress responses in eukaryotes. Golgi anti-apoptotic proteins (GAAPs) are evolutionarily conserved cell death regulators. Human and viral GAAPs inhibit apoptosis and modulate intracellular Ca2+fluxes, and viral GAAPs form cation-selective channels. Although most mammalian cell death regulators are not conserved at the sequence level in plants, the GAAP gene family shows expansion, with five paralogues (AtGAAP1-5) in the Arabidopsis genome. We pursued molecular and physiological characterization of AtGAAPs making use of the advanced knowledge of their human and viral counterparts. Structural modeling of AtGAAPs predicted the presence of a channel-like pore, and electrophysiological recordings from purified AtGAAP3 reconstituted into lipid bilayers confirmed that plant GAAPs can function as ion channels. AtGAAP1 and AtGAAP4 localized exclusively to the Golgi within the plant cell, while AtGAAP2, AtGAAP3 and AtGAAP5 also showed tonoplastic localization. Gene expression analysis revealed differential spatial expression and abundance of transcript forAtGAAPparalogues in Arabidopsis tissues. We demonstrate that AtGAAP1-5 inhibit Bax-induced cell death in yeast. However, overexpression of AtGAAP1 induces cell death inNicotiana benthamianaleaves and lesion mimic phenotype in Arabidopsis. We propose that AtGAAPs function as Golgi-localized ion channels that regulate cell death by affecting ionic homeostasis within the cell.HighlightArabidopsis Golgi anti-apoptotic proteins (GAAPs) share functional conservation with their human and viral counterparts in cell death regulation and ion channel activityAbbreviationsAtGAAP,Arabidopsis thalianaGAAP; BI-1, Bax inhibitor-1; CFP, cyan fluorescent protein; CMLV, camelpox virus; ER, Endoplasmic reticulum; GAAP, Golgi anti-apoptotic protein; GFP, green fluorescent protein; hGAAP, human GAAP; LFG, Lifeguard; LMM, lesion mimic mutant; PCD, programmed cell death; TMBIM, transmembrane Bax inhibitor-1 motif-containing; TMDs, transmembrane domains; vGAAP, viral GAAP; YFP, yellow fluorescent protein

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The contribution of organelles to plant intracellular calcium signalling

Cited by 108 publications

References 241 publications

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

Chloroplast Calcium Signaling in the Spotlight

Golgi anti-apoptotic proteins are evolutionarily conserved ion channels that regulate cell death in plants

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The contribution of organelles to plant intracellular calcium signalling

Cited by 108 publications

References 241 publications

Cellular Ca2+ Signals Generate Defined pH Signatures in Plants

Cellular Ca2+ Signals Generate Defined pH Signatures in Plants

Chloroplast Calcium Signaling in the Spotlight

Golgi anti-apoptotic proteins are evolutionarily conserved ion channels that regulate cell death in plants

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Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants