Regulation of Freezing Tolerance and Flowering in Temperate Cereals: The VRN-1 Connection    

Abstract

In winter wheat (Triticum spp.) and barley (Hordeum vulgare) varieties, long exposures to nonfreezing cold temperatures accelerate flowering time (vernalization) and improve freezing tolerance (cold acclimation). However, when plants initiate their reproductive development, freezing tolerance decreases, suggesting a connection between the two processes. To better understand this connection, we used two diploid wheat (Triticum monococcum) mutants, maintained vegetative phase (mvp), that carry deletions encompassing VRN-1, the major vernalization gene in temperate cereals. Homozygous mvp/mvp plants never flower, whereas plants carrying at least one functional VRN-1 copy (Mvp/-) exhibit normal flowering and high transcript levels of VRN-1 under long days. The Mvp/- plants showed reduced freezing tolerance and reduced transcript levels of several cold-induced C-REPEAT BINDING FACTOR transcription factors and COLD REGULATED genes (COR) relative to the mvp/mvp plants. Diploid wheat accessions with mutations in the VRN-1 promoter, resulting in high transcript levels under both long and short days, showed a significant down-regulation of COR14b under long days but not under short days. Taken together, these studies suggest that VRN-1 is required for the initiation of the regulatory cascade that down-regulates the cold acclimation pathway but that additional genes regulated by long days are required for the down-regulation of the COR genes. In addition, our results show that allelic variation in VRN-1 is sufficient to determine differences in freezing tolerance, suggesting that quantitative trait loci for freezing tolerance previously mapped on this chromosome region are likely a pleiotropic effect of VRN-1 rather than the effect of a separate closely linked locus (FROST RESISTANCE-1), as proposed in early freezing tolerance studies.

Direct links between the vernalization response and other key traits of cereal crops

“…In addition, some targets of VRN1 are likely to show altered expression only under specific conditions. This is known to be the case for CBF genes targeted by VRN1; HvCBF2, HvCBF4 and HvCBF9 have reduced expression during low-temperature treatment in lines with elevated VRN1 activity but are not expressed in normal glasshouse conditions 33 . A key objective for future studies will be global analyses of gene expression in specific organs and cell types, combined with matching ChIP-seq analysis of VRN1 targets.…”

Role of Epigenetic Mechanisms in Plant Response to Low Temperature

“…Numerous studies with near-isogenic lines and QTL mapping studies have pointed to VRN1 as an important regulator of freezing tolerance (Francia et al, 2004;Limin and Fowler, 2006;Galiba et al, 2009). The results indicate that allelic variation in VRN1 is sufficient to determine the differences in the degree of freezing tolerance, suggesting that quantitative trait loci for freezing tolerance previously mapped on this chromosome region are likely a pleiotropic effect of VRN1 rather than the effect of a separate closely linked locus of FR1 (Frost Resistance-1) (Limin and Fowler, 2006;Dhillon et al, 2010). Studies in Arabidopsis thaliana have shown that core histone (mainly H4) acetylation and deacetylation play a key role in gene activation/repression during cold acclimation and freezing tolerance.…”

“…Some experiments conducted with Triticum monococcum mutants with deletion of the VRN1 gene -mpv/mpv (Maintained Vegetative Phase) -showed that homozygous plants (mpv/mpv) cannot flower while heterozygous plants (Mvp/-) carrying one functional VRN1 copy can flower normally. A high level of VRN1 transcription under long-day conditions was detected in heterozygous plants, whereas frost tolerance was reduced as well as the transcription level of many cold-induced genes, among others CBF (also known as Dehydration Responsive Elements) and COR genes (Dhillon et al, 2010). CBF genes encode transcription factors which interact with the conservative CCGAC sequence motif (C-repeat (CRT)/dehydration element DRE) located at promoter sites of many genes involved in early drought and cold response (Galiba et al, 2009).…”

Flow cytometric chromosome sorting from diploid progenitors of bread wheat, T. urartu, Ae. speltoides and Ae. tauschii

“…The VRN1 gene, which is critical for the adaptation of polyploid wheats to autumn sowing and divides wheat varieties into the winter and spring market classes, has been mapped to the colinear regions of the long arm of chromosomes 5A, 5B and 5D (Galiba et al 1995;Snape et al 1997). The group 5 chromosomes of hexaploid wheat also carry major loci affecting winter hardiness and freezing tolerance, designated as FROST RESISTANCE-1 (FR-1; Sutka and Snape 1989) and FR-2, which is approximately 30 centimorgans proximal to VRN-1 and includes a cluster of 11 (or more) C-REPEAT BINDING FACTOR (CBF) genes (Vágújfalvi et al 2003;Dhillon et al 2010). Other loci affecting drought and salt tolerance and the crossability of wheat have also been mapped to group 5 chromosomes (Quarrie et al 1994;Koebner et al 1996;riley and Chapman 1967;Sitch et al 1985;Krolow 1970).…”