Freezing‐sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing‐tolerant Arabidopsis

Abstract

SummaryMany plants increase in freezing tolerance in response to low temperature, a process known as cold acclimation. In Arabidopsis, cold acclimation involves action of the CBF cold response pathway. Key components of the pathway include rapid cold-induced expression of three homologous genes encoding transcriptional activators, CBF1, 2 and 3 (also known as DREB1b, c and a, respectively), followed by expression of CBF-targeted genes, the CBF regulon, that increase freezing tolerance. Unlike Arabidopsis, tomato cannot cold acclimate raising the question of whether it has a functional CBF cold response pathway. Here we show that tomato, like Arabidopsis, encodes three CBF homologs, LeCBF1-3 (Lycopersicon esculentum CBF1-3), that are present in tandem array in the genome. Only the tomato LeCBF1 gene, however, was found to be coldinducible. As is the case for Arabidopsis CBF1-3, transcripts for LeCBF1-3 did accumulate in response to mechanical agitation, but not in response to drought, ABA or high salinity. Constitutive overexpression of LeCBF1 in transgenic Arabidopsis plants induced expression of CBF-targeted genes and increased freezing tolerance indicating that LeCBF1 encodes a functional homolog of the Arabidopsis CBF1-3 proteins. However, constitutive overexpression of either LeCBF1 or AtCBF3 in transgenic tomato plants did not increase freezing tolerance. Gene expression studies, including the use of a cDNA microarray representing approximately 8000 tomato genes, identified only four genes that were induced 2.5-fold or more in the LeCBF1 or AtCBF3 overexpressing plants, three of which were putative members of the tomato CBF regulon as they were also upregulated in response to low temperature. Additional experiments indicated that of eight tomato genes that were likely orthologs of Arabidopsis CBF regulon genes, none were responsive to CBF overexpression in tomato. From these results, we conclude that tomato has a complete CBF cold response pathway, but that the tomato CBF regulon differs from that of Arabidopsis and appears to be considerably smaller and less diverse in function.

Functionality of soybean CBF/DREB1 transcription factors

“…All of these genes have very similar Nuclear Localization Signals (NLS) and AP2 domains followed by an acidic region at C-terminus. Unlike CBF1, 2 and 3 of Arabidopsis and tomato [13,28], the soybean CBF genes are not found as tandem arrays on the same chromosome (Chromosome 4 in Arabidopsis, Chromosome 3 in tomato), but rather were scattered among seven different soybean chromosomes. Soybean is a tetraploid plant, with about 75% of the genes having multiple copies [39].…”

“…The accumulation of downstream genes mediated by CBF/DREB1 genes, increases abiotic stress tolerances to freezing, dehydration, and high salt [14,[20][21][22][23][24]. In cold-intolerant tomato, the transgenic expression of AtCBF1 gene increased cold regulated genes [25] [ 26,27] and the expression of AtCBF1 in tomato increases freezing tolerance [26][27][28].…”

Proteomic Study of Low-Temperature Responses in Strawberry Cultivars (Fragaria×ananassa) That Differ in Cold Tolerance

“…Genes encoding CBFs have been identified in sour cherry (Prunus cerasus) and strawberry (Owens et al, 2002;Kitashiba et al, 2003). However, it is likely that CBF regulons differ in different plants (Zhang et al, 2004). Crucial for surviving freezing temperatures are transcriptional activation and repression of genes, changes in metabolism, activation of scavengers for ROS, alteration of membrane composition, and accumulation of cryoprotective molecules (e.g.…”

Cloning and characterization of cold, salt and drought inducible C-repeat binding factor gene from a highly cold adapted ecotype of Lepidium latifolium L.

“…Phylogentically divergent relationship of LlCBF with other member of the same family may be because of evolutionary modification specifically in non-DNA binding region of the gene to fulfil the functional requirement. Zhang et al (2004b) also opined that the regulon size or the number and kind of target genes vary among freezing sensitive and tolerant plants.…”

“…These studies suggest that ICE1-CBF regulon is conserved in diverse plant species. The regulon size or the number and kind of target genes vary among freezing sensitive and tolerant plants (Zhang et al 2004b). The calmodulin binding transcription activator (CAMTA) family proteins act as transcriptional regulators of CBF2 expression in Arabidopsis.…”