So What's New in the Field of Plant Cold Acclimation? Lots!

Abstract

Due to its intrinsically interesting nature and importance to agriculture, considerable effort has been directed at understanding the phenomenon of “cold acclimation,” the process whereby certain plants increase in freezing tolerance upon exposure to low temperature. By 1980, thousands of research articles had been published on the topic and significant insights had been gained, including the following: Freezing tolerance is a multigenic trait, freezing injury in most plants and tissues results largely from the severe cellular dehydration that occurs upon ice formation, and the cellular membrane systems are a primary site of freeze-induced injury. What was lacking, however, was a consensus regarding the mechanistic basis of freezing tolerance. Moreover, specific genes with functional roles in freezing tolerance had not been identified and their modes of action had not been determined, critical deficiencies in regard to both a basic understanding of cold acclimation and practical efforts to improve the stress tolerance of agronomic plants. Now, 20 years later, the cold acclimation research landscape has dramatically changed. Largely through bringing molecular genetic and mutational approaches to bear on the topic, along with the development of Arabidopsis as a model to study the phenomenon, genes with roles in cold acclimation have begun to be identified and their modes of action determined. In addition, low-temperature signaling and regulatory pathways involved in activating the cold acclimation response have begun to be described and the insights gained are beginning to suggest novel approaches to improve the environmental stress tolerance of plants. My objective here is to highlight some of these exciting advances. In 1985, Guy et al. (4) established that changes in gene expression occur with cold acclimation and so opened a floodgate of effort by investigators to identify and characterize cold-responsive genes (22). The underlying hypothesis was that some of these genes were likely to be involved in freezing tolerance and that studies of their regulation and function would provide new insights into the cold acclimation process. Studies on cold-regulated gene expression in Arabidopsis have resulted in the discovery of a family of transcriptional activators, the CBF/DREB1 proteins, that have a key role in cold acclimation. Model of the Arabidopsis CBF cold acclimation pathway. Low temperature leads to rapid induction of theCBF/DREB1 genes that in turn results in expression of the CBF regulon of CRT/DRE-regulated genes. Action of the CBF regulon, which includes COR, ERD, and presumably yet to be discovered (“XYZ”) cold-regulated genes,results in an increase in plant freezing tolerance. Cold-induced expression of the CBF/DREB1 genes has been proposed (3) to involve the action of a regulatory protein present at warm temperature designated ICE (inducer of CBF expression). Low temperature is envisioned to either activate the ICE protein or other protein(s) with which it interacts (3). Such activation may involve alterations in protein phosphorylation caused by a cold-induced influx of calcium (see text). The SFR6 protein appears to act between CBF/DREB1transcription and induction of the CRT/DRE-regulated genes (11) whereas HOS1 appears to act upstream of CBF transcription (13). Given that the CBF/DREB1 proteins can induce transcription of cold-regulated CRT/DRE-containing target genes without a low-temperature stimulus, why aren't the CRT/DRE-regulated genes normally expressed at warm temperatures? The simple answer is that theCBF/DREB1 genes themselves are cold regulated (3, 14). Within 15 min of transfer to low temperature, CBF/DREB1 transcripts begin to accumulate, followed at 1 to 2 h by accumulation of transcripts for the target CRT/DRE-regulated genes. The mechanism whereby the CBF/DREB1 genes are activated by low temperature is not yet known, but appears to involve the action of cold-responsive promoters (18) that are not subject to autoregulation (3). Thus, Gilmour et al. (3) have hypothesized the existence of a transcription factor, designated ICE, that acts at the CBF/DREB1 promoters (Fig. 1). As envisioned, the protein would be present at normal growth temperature, but be in an inactive state. Upon exposing plants to low temperature, ICE (or a protein that it interacts with) is proposed to become activated and stimulate transcription of theCBF/DREB1 genes followed by induction of the CBF regulon (Fig. 1). As temperatures drop below freezing, ice formation is generally initiated in the extracellular spaces of plants and, because the chemical potential of ice is less than that of liquid water, there is movement of unfrozen water from inside the cell to the extracellular spaces where it freezes. This process continues until an equilibrium in chemical potential is achieved. If the freezing temperature is −10°C, the unfrozen liquid will have an osmolarity of about 5 and typically greater than 90% of the o