The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements

Joyce C Pennycooke, Hongmei Cheng, Stephanie M Roberts, Qiaofeng Yang, Seung Y Rhee, Eric J Stockinger
Plant Molecular Biology 2008, 67 (5): 483-97
Some plants like Arabidopsis thaliana increase in freezing tolerance when exposed to low nonfreezing temperatures, a process known as cold acclimation. Other plants including tomato, Solanum lycopersicum, are chilling sensitive and incur injury during prolonged low temperature exposure. A key initial event that occurs upon low temperature exposure is the induction of genes encoding the CBF transcription factors. In Arabidopsis three CBF genes, present in a tandemly-linked cluster, are induced by low temperatures. Tomato also harbors three tandemly-linked CBF genes, Sl-CBF3-CBF1-CBF2, but only one of these, Sl-CBF1, is low-temperature responsive. Here we report that Solanum species that are closely-allied to cultivated tomato essentially share this structural organization, but the locus is in a dynamic state of flux. Additional paralogs and in-frame deletions between adjacent genes occur, and the genomic regions flanking the CBF genes are dissimilar across Solanum species. Nevertheless, the CBF1 upstream region remains intact and highly conserved. This feature differed for CBF2 and CBF3, whose upstream regions were far less conserved. CBF1 was also the only low-temperature responsive gene in the cluster and its expression was greatly affected by a circadian clock. The tuber-bearing S. tuberosum and S. commersonii also harbored a fourth gene, CBF4, which was also low temperature responsive. CBF4 was physically linked to CBF5 in S. tuberosum, but CBF5 was absent from S. commersonii. Phylogenic analyses suggest that CBF5-CBF4 resulted from the duplication of the CBF3-CBF1-CBF2 cluster. DNA sequence motifs shared between the Solanum CBF1 and CBF4 upstream regions were identified, portions of which were also present in the Arabidopsis CBF1-3 upstream regions. These results suggest that much greater functional constraints are placed upon the Solanum CBF1 upstream regions over the other CBF upstream regions and that CBF4 has retained the capacity for low temperature responsiveness following the duplication event that gave rise to CBF4.

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