Cold acclimation is affected by diurnal cycles and minute-scale random temperature fluctuations via calcium signals
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Molecular and physiological processes during cold acclimation (CA) have been investigated using plants incubated under constant low-temperature conditions. However, to comprehensively characterize CA in the field, the effects of day–night temperature cycles and minute-scale random temperature fluctuations must be clarified. Thus, we developed an experimental system that can maintain diurnal cycles and random temperature fluctuations during CA treatments. On the basis of the temperature changes in the field, three CA conditions were applied: conventional CA at 2°C (con-CA), CA with a 10°C day/2°C night cycle (C-CA), and C-CA with random temperature fluctuations only during the day (FC-CA). Because cold-induced Ca 2+ signals help regulate CA, the effects of Ca 2+ signals during the three CA treatments were examined using Ca 2+ channel blockers (LaCl 3 and ruthenium red). The freezing tolerance of Arabidopsis thaliana was similar after the C-CA and con-CA treatments, but it decreased following the FC-CA treatment. The analysis of transcription factors regulating CA processes indicated CBF/DREB1 expression levels tended to be highest for the con-CA treatment, followed by the FC-CA and C-CA treatments. Moreover, the Ca 2+ signals substantially contributed to the freezing tolerance of the plants that underwent the FC-CA and C-CA treatments, while also considerably modulating gene expression in the FC-CA-treated plants. Furthermore, the Ca 2+ signals enhanced CBF/DREB1 expression during the FC-CA treatment, but the Ca 2+ signals derived from intracellular organelles suppressed the expression of CBF2/DREB1C and CBF3/DREB1A during the C-CA treatment. Thus, diurnal temperature cycles and random temperature fluctuations affect CA through different calcium signals, implying that plants regulate CA by precisely sensing temperature changes in the field.Keywords:
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The effects of ruthenium red, pH, and sodium ions on active and passive Ca2+ transport were studied in digitonin-treated (0.1 mg/ml) suspension of myometrial cells using radiolabeled 45Ca2+. The inhibitor of mitochondrial Ca2+ accumulation ruthenium red (10 microM) suppressed active accumulation of the cation in permeabilized myocytes by 78-85%. Ruthenium red-sensitive Ca2+ accumulation significantly (10-fold, mean) exceeds ruthenium red-resistant Mg2+, ATP-dependent Ca2+ accumulation assayed in the absence of oxalate and inhibited by 50 nM tapsigargin (blocker of endo/sarcoplasmic reticulum calcium pump). Acidification of incubation medium (pH 8.0-6.0, Tris-malcate/KOH buffer) inhibits ruthenium red-sensitive active Ca2+ accumulation in permeabilized myocytes and passive release of this cation in the dilution medium after blockage of mitochondrial Ca2+ accumulation by ruthenium red. Partial isotonic substitution of KCl (135-95 mM) with NaCl (15-55 mM) in incubation medium did not affect the initial rate of active ruthenium red-sensitive Ca2+ accumulation and the kinetics of passive Ca2+ release from permeabilized cells after blockade of active Ca2+ accumulation by ruthenium red. Mechanism of Ca2+ exchange in myometrial mitochondria is discussed.
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Ruthenium red prevented the spontaneous calcium release and the accompanying mitochondrial destruction occurring in calcium-loaded mitochondria in the presence of phosphate. Under these conditions delta pH and membrane potential delta psi were preserved and the ruthenium red-induced calcium efflux was low and at a constant rate. On prolonged incubation with calcium prior to addition of ruthenium red increasingly more mitochondrial calcium developed into a pool rapidly dischargeable by ruthenium red. This development was accompanied by stimulation of respiration which was, however, not abolished by ruthenium red as could have been expected if it had been caused by calcium cycling. Calcium therefore altered mitochondria by a different mechanism than by cycling across the inner membrane.
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Article On the State of Calcium Ions in Isolated Rat Liver Mitochondria. III. Diversity of Ruthenium Red Action on Different Calcium Pools was published on January 1, 1984 in the journal Biological Chemistry (volume 365, issue 2).
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