Calcium signals: the lead currency of plant information processing

Abstract

Ca(2+) signals are core transducers and regulators in many adaptation and developmental processes of plants. Ca(2+) signals are represented by stimulus-specific signatures that result from the concerted action of channels, pumps, and carriers that shape temporally and spatially defined Ca(2+) elevations. Cellular Ca(2+) signals are decoded and transmitted by a toolkit of Ca(2+) binding proteins that relay this information into downstream responses. Major transduction routes of Ca(2+) signaling involve Ca(2+)-regulated kinases mediating phosphorylation events that orchestrate downstream responses or comprise regulation of gene expression via Ca(2+)-regulated transcription factors and Ca(2+)-responsive promoter elements. Here, we review some of the remarkable progress that has been made in recent years, especially in identifying critical components functioning in Ca(2+) signal transduction, both at the single-cell and multicellular level. Despite impressive progress in our understanding of the processing of Ca(2+) signals during the past years, the elucidation of the exact mechanistic principles that underlie the specific recognition and conversion of the cellular Ca(2+) currency into defined changes in protein-protein interaction, protein phosphorylation, and gene expression and thereby establish the specificity in stimulus response coupling remain to be explored.

Figure 1.

Ca²⁺ Signaling in Guard Cell Regulation. (A) Schematic representation of artificially imposed Ca²⁺ oscillations/plateau and the corresponding temporal changes in stomatal aperture. The long-term Ca²⁺-programmed closure is caused by Ca²⁺ oscillations with a defined pattern (Ca²⁺ signature), whereas the short-term Ca²⁺-reactive closure is induced by [Ca²⁺]_cyt elevation, regardless of the pattern. (B) Simplified model for Ca²⁺ controlled stomatal closure and opening. Stomatal closing stimuli, such as ABA, high CO₂, and cold, induce spontaneous Ca²⁺ oscillations, resulting in Ca²⁺-reactive closure and subsequent Ca²⁺-programmed closure. On the other hand, low CO₂-induced Ca²⁺ oscillations result not in Ca²⁺-reactive closure but stomatal opening, implying that the stimulus may desensitize the signaling pathways of the Ca²⁺-reactive closure (Ca²⁺ sensitivity priming hypothesis). It is unknown whether low CO₂-induced Ca²⁺ oscillation itself encrypts specific information of stomatal opening.

Figure 2.

Overview of Ca²⁺ Transport Systems in an Arabidopsis Cell. Shown are Ca²⁺ influx/efflux pathways that have been identified at the molecular level. See text for further details. CNGC, cyclic nucleotide channel; GLR, glutamate receptor; TPC1, two pore channel 1; CAS, Ca²⁺-sensing receptor; ACA, autoinhibited calcium ATPase; ECA, ER type calcium ATPase; HMA1, heavy metal ATPase1; CAX, cation exchanger.

Figure 3.

The CDPK Signaling System for Translating Ca²⁺ Signatures into Protein Phosphorylation. Shown are characterized components of the CDPK system. See text for further details. RSG, repression of shoot growth; ABF, ABA response element-binding factor.

Figure 4.

The CBL/CIPK Signaling System for Translating Ca²⁺ Signatures into Protein Phosphorylation. Shown are characterized complexes consisting of CBL proteins and their interacting CIPKs. AKT1, Arabidopsis K⁺ transporter 1; SOS1, salt overly sensitive 1; CHL, a nitrate transporter; AHA2, Arabidopsis H⁺ ATPase 2.

Figure 5.

Converting Ca²⁺ Signals into Transcriptional Responses. Recent studies have unveiled that Ca²⁺/CAMs (calmodulins) regulate CAMTAs that interact with promoters of abiotic stress-responsive genes. Interestingly, Arabidopsis CAM7 is likely a direct converter of cytoplasmic Ca²⁺ signatures into regulation of gene expression. EDS1, enhanced disease susceptibility 1.