Cold Calcium Signaling in Arabidopsis Involves Two Cellular Pools and a Change in Calcium Signature after Acclimation

Abstract

Cold shock elicits an immediate rise in cytosolic free calcium concentration ([Ca2+]cyt) in both chilling-resistant Arabidopsis and chilling-sensitive tobacco (Nicotiana plumbaginifolia). In Arabidopsis, lanthanum or EGTA caused a partial inhibition of both cold shock [Ca2+]cyt elevation and cold-dependent kin1 gene expression. This suggested that calcium influx plays a major role in the cold shock [Ca2+]cyt response and that an intracellular calcium source also might be involved. To investigate whether the vacuole (the major intracellular calcium store in plants) is involved, we targeted the calcium-dependent photoprotein aequorin to the cytosolic face of the vacuolar membrane. Cold shock calcium kinetics in this microdomain were consistent with a cold-induced vacuolar release of calcium. Treatment with neomycin or lithium, which interferes with phosphoinositide cycling, resulted in cold shock [Ca2+]cyt kinetics consistent with the involvement of inositol trisphosphate and inositide phosphate signaling in this response. We also investigated the effects of repeated and prolonged low temperature on cold shock [Ca2+]cyt. Differences were observed between the responses of Arabidopsis and N. plum-baginifolia to repeated cold stimulation. Acclimation of Arabidopsis by pretreatment with cold or hydrogen peroxide caused a modified calcium signature to subsequent cold shock. This suggests that acclimation involves modification of plant calcium signaling to provide a "cold memory."

Transcriptome response to temperature stress in the wolf spider Pardosa pseudoannulata (Araneae: Lycosidae)

“…Numerous studies have demonstrated that Ca 2+ plays a vital role in the cold‐stress response of plants, for example in Arabidopsis (Knight et al. 1996; Polisensky and Braam 1996; Jakoby et al. 2002), banana (Yang et al.…”

Cold Induction of Arabidopsis CBF Genes Involves Multiple ICE (Inducer of CBF Expression) Promoter Elements and a Cold-Regulatory Circuit That Is Desensitized by Low Temperature

“…However, a "cold memory" has been described for coldinduced calcium flux in Arabidopsis (Knight et al, 1996). Transfer of Arabidopsis plants to low temperatures results in a rapid, transient increase in free calcium in the cytoplasm, which comes from extracellular and intracellular calcium stores (Knight et al, 1996;Knight and Knight, 2000). Knight et al (1996) have shown that the calcium signature-the peak levels and duration of the calcium influx-is altered upon cold acclimation, becoming diminished in magnitude and prolonged in length.…”

“…Transfer of Arabidopsis plants to low temperatures results in a rapid, transient increase in free calcium in the cytoplasm, which comes from extracellular and intracellular calcium stores (Knight et al, 1996;Knight and Knight, 2000). Knight et al (1996) have shown that the calcium signature-the peak levels and duration of the calcium influx-is altered upon cold acclimation, becoming diminished in magnitude and prolonged in length. The significance here is that the expression of certain cold-regulated genes, including COR and other CBF-targeted genes, appears to involve the action of calcium as second messenger.…”

“…However, a "cold memory" has been described for coldinduced calcium flux in Arabidopsis (Knight et al, 1996). Transfer of Arabidopsis plants to low temperatures results in a rapid, transient increase in free calcium in the cytoplasm, which comes from extracellular and intracellular calcium stores (Knight et al, 1996;Knight and Knight, 2000).…”

Fluorescence Resonance Energy Transfer-Sensitized Emission of Yellow Cameleon 3.60 Reveals Root Zone-Specific Calcium Signatures in Arabidopsis in Response to Aluminum and Other Trivalent Cations

“…Such measurements have been conducted using Ca 2+ -sensitive fluorescent indicator dyes (e.g. Indo and Fura), the luminescent protein aequorin (Knight et al, 1991(Knight et al, , 1996Legué et al, 1997;Wymer et al, 1997;Cárdenas et al, 2008), and more recently the yellow cameleon (YC) Ca 2+ sensor, a chimeric protein that relies on fluorescence resonance energy transfer (FRET) as an indicator of [Ca 2+ ] cyt changes in the cell (Allen et al, 1999;Miwa et al, 2006;Qi et al, 2006;Tang et al, 2007;Haruta et al, 2008). The YC reporter is composed of cyan fluorescent protein (CFP), the C terminus of calmodulin (CaM), a Gly-Gly linker, the CaM-binding domain of myosin light chain kinase (M13), and a yellow fluorescent protein (YFP; Miyawaki et al, 1997Miyawaki et al, , 1999.…”