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Rapid Transcriptome Changes Induced by Cytosolic Ca²⁺ Transients Reveal ABRE-Related Sequences as Ca²⁺-Responsive cis Elements in Arabidopsis^[W]

^a Department of Plant Sciences, Weizmann Institute of Science, Rehovot 76100, Israel
^b Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom
^c Department of Plant Sciences, Faculty of Life Sciences, Tel Aviv University, 69978 Tel Aviv, Israel

² To whom correspondence should be addressed. E-mail hillelf{at}post.tau.ac.il; fax 972-36406816.

The regulation of gene expression by cellular calcium is crucial for plant defense against biotic and abiotic stresses. However, the number of genes known to respond to specific transient calcium signals is limited, and as yet there is no definition of a calcium-responsive cis element in plants. Here, we generated specific cytosolic calcium transients in intact Arabidopsis thaliana seedlings and linked them to early transcriptome changes, followed by bioinformatic analysis of the responsive genes. A cytosolic calcium transient induced by calmodulin antagonists and blocked by lanthanides was characterized using aequorin-based luminometry and photon imaging. Analysis of transcriptome changes revealed 230 calcium-responsive genes, of which 162 were upregulated and 68 were downregulated. These include known early stress-responsive genes as well as genes of unknown function. Analysis of their upstream regions revealed, exclusively in the upregulated genes, a highly significant occurrence of a consensus sequence (P < 10^–13) comprising two abscisic acid–specific cis elements: the abscisic acid–responsive element (ABRE; CACGTG[T/C/G]) and its coupling element ([C/A]ACGCG[T/C/A]). Finally, we show that a tetramer of the ABRE cis element is sufficient to confer transcriptional activation in response to cytosolic Ca²⁺ transients. Thus, at least for some specific Ca²⁺ transients and motif combinations, ABREs function as Ca²⁺-responsive cis elements.

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