Large deletions in the CBF gene cluster at the Fr-B2 locus are associated with reduced frost tolerance in wheat

Abstract

Wheat plants which are exposed to periods of low temperatures (cold acclimation) exhibit increased survival rates when they are subsequently exposed to freezing temperatures. This process is associated with large-scale changes in the transcriptome which are modulated by a set of tandemly duplicated CBF (C-repeat Binding Factor) transcription factors located at the Fr-2 (Frost Resistance-2) locus. While Arabidopsis has three tandemly duplicated CBF genes, the CBF family in wheat has undergone an expansion and at least 15 CBF genes have been identified, eleven of which are present at the Fr-2 loci on homoeologous group 5 chromosomes. We report here the discovery of three large deletions which eliminate six, nine, and all eleven CBF genes from the Fr-B2 locus in tetraploid and hexaploid wheat. In wild emmer wheat, the Fr-B2 deletions were found only among the accessions from the southern sub-populations. Among cultivated wheats, the Fr-B2 deletions were more common among varieties with a spring growth habit than among those with a winter growth habit. Replicated freezing tolerance experiments showed that both the deletion of nine CBF genes in tetraploid wheat and the complete Fr-B2 deletion in hexaploid wheat are associated with significant reductions in survival after exposure to freezing temperatures. Our results suggest that selection for the wild type Fr-B2 allele may be beneficial for breeders selecting for varieties with improved frost tolerance.

Copy number variation at the HvCBF4–HvCBF2 genomic segment is a major component of frost resistance in barley

“…In fact, even though mutations within individual CBF-coding sequences were firstly proposed as causative of frost resistance variation in diploid wheat (Knox et al 2008), a differential expansion of the gene cluster together with copy number variation (CNV), has been put forward as a structural explanation for the functional role played by the CBFs at FR-2 in different genotypes. Evidences in favour of this hypothesis start to accumulate in barley and hexaploid wheat Pearce et al 2013;Jeknić et al 2014;Zhu et al 2014).…”

“…durum) and hexaploid (T. aestivum) bread wheat (Pearce et al 2013). Increased copy number of the central cluster has also been observed, and this was frequently associated with haplotype variation at VRN-A1 and with higher TaCBF-A14 transcript levels .…”

Advances in physiological and molecular aspects of plant cold tolerance

“…Cold acclimation is defined as the exposure of plants to low non-freezing temperatures leading to significant positive effect on the cold tolerance of the plants (Thomashow 2010;Pearce et al 2013). Extensive researches have been conducted to improve the understanding of the biochemical and molecular basis of the cold acclimation response and the changes that take place throughout this process (Lissarre et al 2010).…”

“…The authors reported that the analysis of the relationship between different types of CBFs revealed a tight co-regulation between CBF1 and CBF3, whereas the relationship between CBF2 and CBF1 or CBF3 expression levels was intensely related to the genetic background of the RNAi lines. However, while three closely related CBF genes have been reported in Arabidopsis, wheat and some other cereals have undertaken an extension in this family (Pearce et al 2013). Badawi et al (2007) reported that there are at least 15 CBF genes in each of the three hexaploid wheat genomes.…”

The Arabidopsis Mediator Complex Subunits MED16, MED14, and MED2 Regulate Mediator and RNA Polymerase II Recruitment to CBF-Responsive Cold-Regulated Genes

“…In wild-type plants, expression of COR genes whose promoters contain the C-repeat motif (CRT; or drought-responsive element [DRE]) (Yamaguchi-Shinozaki and Shinozaki, 1994) is upregulated in response to cold by the action of the AP2 transcription factors C-repeat binding factor1 (CBF1), CBF2, and CBF3 (Stockinger et al, 1997;Gilmour et al, 2004), also known as DREB1B, DREB1C and DREB1A, respectively (Liu et al, 1998). The CBFs are essential regulators of freezing tolerance across a range of monocotyledonous as well as dicotyledonous species (Jaglo et al, 2001;Badawi et al, 2007;Pearce et al, 2013).…”