Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene

Abstract

Prolonged exposure to low temperatures (vernalization) accelerates the transition to reproductive growth in many plant species, including the model plant Arabidopsis thaliana and the economically important cereal crops, wheat and barley. Vernalizationinduced flowering is an epigenetic phenomenon. In Arabidopsis, stable down-regulation of FLOWERING LOCUS C (FLC) by vernalization is associated with changes in histone modifications at FLC chromatin. In cereals, the vernalization response is mediated by stable induction of the floral promoter VERNALIZATION1 (VRN1), which initiates reproductive development at the shoot apex. We show that in barley (Hordeum vulgare), repression of HvVRN1 before vernalization is associated with high levels of histone 3 lysine 27 trimethylation (H3K27me3) at HvVRN1 chromatin. Vernalization caused increased levels of histone 3 lysine 4 trimethylation (H3K4me3) and a loss of H3K27me3 at HvVRN1, suggesting that vernalization promotes an active chromatin state at VRN1. Levels of these histone modifications at 2 other floweringtime genes, VERNALIZATION2 and FLOWERING LOCUS T, were not altered by vernalization. Our study suggests that maintenance of an active chromatin state at VRN1 is likely to be the basis for epigenetic memory of vernalization in cereals. Thus, regulation of chromatin state is a feature of epigenetic memory of vernalization in Arabidopsis and the cereals; however, whereas vernalizationinduced flowering in Arabidopsis is mediated by epigenetic regulation of the floral repressor FLC, this phenomenon in cereals is mediated by epigenetic regulation of the floral activator, VRN1.epigenetic ͉ MADS ͉ intron ͉ barley ͉ chromatin P lants respond to seasonal cues, such as temperature and day-length, to ensure that flowering coincides with favorable conditions. Prolonged exposure to low winter temperatures (vernalization) accelerates the progression from vegetative to reproductive growth in many plant species, including the temperate cereals (such as wheat and barley) and dicot species (such as Arabidopsis) (1-3). In both these lineages, plants retain a ''memory'' of the prolonged cold of winter, which stimulates flowering when days lengthen during spring (1-3). The memory of cold is then reset in the next sexual generation to ensure progeny are competent to respond to vernalization (1-3).In Arabidopsis, the vernalization response is mediated by epigenetic regulation of the floral repressor, FLOWERING LOCUS C (FLC), which encodes a MADS-box transcription factor that represses genes involved in floral initiation, including SUPPRESSOR OF CONSTANS 1 and FLOWERING LOCUS T (FT) (1,(4)(5)(6). FLC is expressed before vernalization and delays flowering, but its expression is repressed by vernalization (1, 4). FLC remains repressed when plants are subsequently exposed to warm temperatures, allowing activation of FT, which promotes flowering (1, 4). The stable down-regulation of FLC by vernalization is associated with an increase in the levels of repressive histone modifications at FLC chromat...

PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod

“…VRN2 and PPD1 compete for the activation of FT1, but the repressing effect of VRN2 is epistatic to the promoting effect of PPD1, preventing flowering in the fall. Long exposures to cold temperatures during the winter (vernalization) result in the up-regulation of VRN1 in both apices and leaves (19,75). In the apex, VRN1 initiates the transition of the shoot apical meristem to the reproductive stage whereas, in the leaves, it acts as a transcriptional repressor of VRN2 (21).…”

Epigenetics in plant tissue culture

“…In plants some epigenetic changes may survive sexual propagation change, viz., through histone modifications (Bastow et al 2004;Kim et al 2009). Interestingly, in barley it is mediated by different histone modifications at the floral activator gene VERNALIZATION1 (VRN1), allowing it to become active (Oliver et al 2009) Another example is the phase change from juvenile to adult, which is paralleled by changes in gross DNA methylation .…”

Vrn-D4 is a vernalization gene located on the centromeric region of chromosome 5D in hexaploid wheat

“…Natural insertions or deletions (indels) in regulatory regions of the three homoeologous genes found in hexaploid wheat (Vrn-A1, Vrn-B1, and Vrn-D1) are associated with dominant alleles for spring growth habit (Fu et al 2005;Yan et al 2004a). During vernalization, these regulatory regions show changes in histone methylation and acetylation associated with the transition between repressed and active chromatin states (Oliver et al 2009). DiVerent combinations of Vrn-A1, Vrn-B1, and Vrn-D1 dominant alleles are the most common sources of spring growth habit among landraces and commercial cultivars of polyploid wheat around the world (Fu et al 2005;Iqbal et al 2007;Iwaki et al 2000Iwaki et al , 2001Stelmakh 1987b;Yan et al 2004a;Zhang et al 2008).…”