In vivo analysis of the calcium signature in the plant Golgi apparatus reveals unique dynamics

Ordenes, Viviana R.; Moreno, Ignacio; Maturana, Daniel; Norambuena, Lorena; Trewavas, Anthony; Orellana, Ariel

doi:10.1016/j.ceca.2012.06.008

Cited by 27 publications

(23 citation statements)

References 48 publications

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“…These SnRK2s are also activated under salt stress and relocate from the root epidermal cytosol to the PM; loss of function impairs root growth (McLoughlin et al, 2012). Work using Golgi-targeted aequorin in Arabidopsis seedlings has shown that an increase in Golgi [Ca 2+ ] follows the [Ca 2+ ] cyt increase induced by hyperosmotic stress, suggesting that this organelle helps terminate the [Ca 2+ ] cyt signal (Ordenes et al, 2012). …”

Section: Water Availability Is Signaled Through [Ca2+]cytmentioning

confidence: 99%

“…This signature would be driven by the opening of plasma membrane (PM) and endomembrane Ca 2+ -permeable channels and terminated by the activity of Ca 2+ efflux transporters in those membranes, plus Ca 2+ -binding proteins, to restore the resting [Ca 2+ ] cyt of 100–200 nM. Use of organelle-targeted Ca 2+ reporting proteins has shown that the Ca 2+ content of the endoplasmic reticulum (ER) and Golgi increases after stress-induced transient increases in [Ca 2+ ] cyt , strongly suggesting that Ca 2+ is sequestered there to terminate the [Ca 2+ ] cyt signal (Ordenes et al, 2012; Bonza et al, 2013). Transport of Ca 2+ into organelles is catalyzed by Ca 2+ -ATPases.…”

Section: Introductionmentioning

confidence: 99%

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Calcium-Mediated Abiotic Stress Signaling in Roots

et al. 2016

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Roots are subjected to a range of abiotic stresses as they forage for water and nutrients. Cytosolic free calcium is a common second messenger in the signaling of abiotic stress. In addition, roots take up calcium both as a nutrient and to stimulate exocytosis in growth. For calcium to fulfill its multiple roles must require strict spatio-temporal regulation of its uptake and efflux across the plasma membrane, its buffering in the cytosol and its sequestration or release from internal stores. This prompts the question of how specificity of signaling output can be achieved against the background of calcium’s other uses. Threats to agriculture such as salinity, water availability and hypoxia are signaled through calcium. Nutrient deficiency is also emerging as a stress that is signaled through cytosolic free calcium, with progress in potassium, nitrate and boron deficiency signaling now being made. Heavy metals have the capacity to trigger or modulate root calcium signaling depending on their dose and their capacity to catalyze production of hydroxyl radicals. Mechanical stress and cold stress can both trigger an increase in root cytosolic free calcium, with the possibility of membrane deformation playing a part in initiating the calcium signal. This review addresses progress in identifying the calcium transporting proteins (particularly channels such as annexins and cyclic nucleotide-gated channels) that effect stress-induced calcium increases in roots and explores links to reactive oxygen species, lipid signaling, and the unfolded protein response.

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Section: Water Availability Is Signaled Through [Ca2+]cytmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Calcium-Mediated Abiotic Stress Signaling in Roots

et al. 2016

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“…Indeed, it was shown that at least some of the seven members of the VSR family in Arabidopsis exhibit Ca 2+ -dependent binding to ligands (Watanabe et al, 2002(Watanabe et al, , 2004. It was recently shown that the concentration of Ca 2+ in Golgi is ;0.7 µM (Ordenes et al, 2012), much lower than that in the ER where Ca 2+ concentrations are in the mM range.…”

Section: Binding and Phmentioning

confidence: 99%

In Vivo Intracellular pH Measurements in Tobacco andArabidopsisReveal an Unexpected pH Gradient in the Endomembrane System

Martinière

Bassil

Jublanc³

et al. 2013

The Plant Cell

159

161

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The pH homeostasis of endomembranes is essential for cellular functions. In order to provide direct pH measurements in the endomembrane system lumen, we targeted genetically encoded ratiometric pH sensors to the cytosol, the endoplasmic reticulum, and the trans-Golgi, or the compartments labeled by the vacuolar sorting receptor (VSR), which includes the transGolgi network and prevacuoles. Using noninvasive live-cell imaging to measure pH, we show that a gradual acidification from the endoplasmic reticulum to the lytic vacuole exists, in both tobacco (Nicotiana tabacum) epidermal (DpH 21.5) and Arabidopsis thaliana root cells (DpH 22.1). The average pH in VSR compartments was intermediate between that of the transGolgi and the vacuole. Combining pH measurements with in vivo colocalization experiments, we found that the trans-Golgi network had an acidic pH of 6.1, while the prevacuole and late prevacuole were both more alkaline, with pH of 6.6 and 7.1, respectively. We also showed that endosomal pH, and subsequently vacuolar trafficking of soluble proteins, requires both vacuolar-type H + ATPase-dependent acidification as well as proton efflux mediated at least by the activity of endosomal sodium/proton NHX-type antiporters.

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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%

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

Sierla

Prole

Saraiva

et al. 2019

Preprint

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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

show abstract

In vivo analysis of the calcium signature in the plant Golgi apparatus reveals unique dynamics

Cited by 27 publications

References 48 publications

Calcium-Mediated Abiotic Stress Signaling in Roots

Calcium-Mediated Abiotic Stress Signaling in Roots

In Vivo Intracellular pH Measurements in Tobacco andArabidopsisReveal an Unexpected pH Gradient in the Endomembrane System

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

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