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

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Abstract

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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Abbreviations

CBF:

C-repeat binding factor

CBF/DREB1:

C-repeat binding factor/dehydration responsive element binding 1

CDS:

Coding sequence

CRT/DRE:

C-repeat/dehydration responsive element

HC:

Hydrophobic cluster

ICEr:

Induction of CBF expression region

ZT:

Zeitgeber time

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Acknowledgements

We thank David M. Francis, Esther van der Knaap, David E. Somers and Sophien Kamoun for helpful suggestions during the preparation of the manuscript. This work was supported by grants from the National Science Foundation Plant Genome Project (grant no. 0110124). Salaries and research support were also provided in part by state and federal funds appropriated to the Ohio Agricultural Research and development Center, The Ohio State University.

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  1. Hongmei Cheng

    Present address: Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

Authors and Affiliations

  1. Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center (OARDC), Wooster, OH, 44691, USA

    Joyce C. Pennycooke, Hongmei Cheng, Stephanie M. Roberts & Eric J. Stockinger

  2. Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, 94305, USA

    Qiaofeng Yang & Seung Y. Rhee

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  1. Joyce C. Pennycooke
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Correspondence to Eric J. Stockinger.

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Fig. S1

Solanum CBF polypeptides in BOXSHADE-formatted alignment. The green, fuchsia, and blue boxes identify the CBF1 SER (S), the CBF2 ARG (R), and the CBF3 ARG-ALA-ASN-HIS-SER (RANHS) blocks, respectively. The orange box at the very NH3-termini of CBF polypeptides identifies the amino acid region shared between the CBF1 orthologs and the potato-clade CBF3, and tomato-clade CBF2 orthologs. The turquoise box identifies the abbreviated NH3-termini common to both CBF4 and CBF5 polypeptides. The violet box inclusive of and proximal to HC2 identifies amino acid residues shared between the tomato-clade CBF1 and CBF2 polypeptides that are distinct from the potato-clade CBF1 and CBF2, whereas the lime box between the E-rich motif and HC2 identifies additional residues present in- and shared across the potato-clade CBF1 and CBF2 polypeptides (and also with St-CBF4) that absent from the tomato-clade CBF1 and CBF2 polypeptides. Asterisks above the alignment identify shared residues between CBF3 and CBF5 polypeptides that are distinct from the other CBF polypeptides. The downward black arrow identifies the AP2 domain ARG residue in all tomato-clade CBFs that is a MET residue in all potato-clade CBFs. The downward red arrow identifies the junction point of the Sp-CBF1/2 fusion (DOC 73.5 kb)

Fig. S2

DNA blot hybridizations of S. commersonii (cmm) and S. tuberosum (tbr) DNAs with gene-specific CBF probes. Hybridization probes are indicated above the lanes. B = Bgl I, E = Eco RI, V = Eco RV, X = Xba I. (The additional fragment cross-hybridizing with CBF2 in the Xba I lane results from an Xba I site dividing the region used as probe (TIF 1404 kb)

Fig. S3

Solanum CBF upstream regions in BOXSHADE-formatted sequence alignment. S3A, Alignment of the Solanum CBF1 ortholog upstream regions and portions of the CBF4 upstream regions sharing identity with the CBF1 gene regions. CBF1 sequences begin at the termination codon of the upstream CBF3 gene and continue to the AUG initiator codon (denoted as +1). S. tuberosum CBF4 upstream nucleotides −2048 to −3333 are included in the alignment (i.e., nucleotides −1 to −2048 upstream of CBF4 are omitted). Similarly, only S. commersonii upstream nucleotides −2366 to −2170 are included in the alignment. S3B, Solanum CBF2 upstream regions. S3C, Solanum CBF3 upstream regions. S3D, Alignment of the Sc-CBF4 and St-CBF4 upstream regions. Boxed regions are described in the text (DOC 576 kb)

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Pennycooke, J.C., Cheng, H., Roberts, S.M. et al. The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements. Plant Mol Biol 67, 483–497 (2008). https://doi.org/10.1007/s11103-008-9333-5

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