Vernalization is an environmentally-induced epigenetic switch in which winter cold triggers epigenetic silencing of floral repressors and thus provides competence to flower in spring. In Arabidopsis, winter cold triggers enrichment of tri-methylated histone H3 Lys(27) at chromatin of the floral repressor, FLOWERING LOCUS C (FLC), and results in epigenetically stable repression of FLC. This epigenetic change is mediated by an evolutionarily conserved repressive complex, polycomb repressive complex 2 (PRC2). Here, we show that a long intronic noncoding RNA [termed COLD ASSISTED INTRONIC NONCODING RNA (COLDAIR)] is required for the vernalization-mediated epigenetic repression of FLC. COLDAIR physically associates with a component of PRC2 and targets PRC2 to FLC. Our results show that COLDAIR is required for establishing stable repressive chromatin at FLC through its interaction with PRC2.
In biennials and winter annuals, flowering is typically blocked in the first growing season. Exposure to the prolonged cold of winter, through a process called vernalization, is required to alleviate this block and permit flowering in the second growing season. In winter-annual types of Arabidopsis thaliana, a flowering repressor, FLOWERING LOCUS C (FLC), is expressed at levels that inhibit flowering in the first growing season. Vernalization promotes flowering by causing a repression of FLC that is mitotically stable after return to warm growing conditions. Here we identify a gene with a function in the measurement of the duration of cold exposure and in the establishment of the vernalized state. We show that this silencing involves changes in the modification of histones in FLC chromatin.
Plants have evolved many systems to sense their environment and to modify their growth and development accordingly. One example is vernalization, the process by which flowering is promoted as plants sense exposure to the cold temperatures of winter. A requirement for vernalization is an adaptive trait that helps prevent flowering before winter and permits flowering in the favorable conditions of spring. In Arabidopsis and cereals, vernalization results in the suppression of genes that repress flowering. We describe recent progress in understanding the molecular basis of this suppression. In Arabidopsis, vernalization involves the recruitment of chromatin-modifying complexes to a clade of flowering repressors that are silenced epigenetically via histone modifications. We also discuss the similarities and differences in vernalization between Arabidopsis and cereals.
Vernalization is the process by which sensing a prolonged exposure to winter cold leads to competence to flower in the spring. In winter annual Arabidopsis thaliana accessions, flowering is suppressed in the fall by expression of the potent floral repressor FLOWERING LOCUS C (FLC). Vernalization promotes flowering via epigenetic repression of FLC. Repression is accompanied by a series of histone modifications of FLC chromatin that include dimethylation of histone H3 at Lys9 (H3K9) and Lys27 (H3K27). Here, we report that A. thaliana LIKE HETEROCHROMATIN PROTEIN 1 (LHP1) is necessary to maintain the epigenetically repressed state of FLC upon return to warm conditions typical of spring. LHP1 is enriched at FLC chromatin after prolonged exposure to cold, and LHP1 activity is needed to maintain the increased levels of H3K9 dimethylation at FLC chromatin that are characteristic of the vernalized state.
The proper timing of flowering is critical for successful reproduction. The perception of the seasonal cues of daylength changes and exposure to cold influences flowering time in many plant species through the photoperiod and vernalization pathways, respectively. Here we show that a plant homeodomain (PHD) finger-containing protein, VIN3-LIKE 1 (VIL1), participates in both the photoperiod and vernalization pathways in Arabidopsis thaliana by regulating expression of the related floral repressors FLOWERING LOCUS C (FLC) and FLOWERING LO-CUS M (FLM). In the vernalization pathway, VIL1, along with VERNALIZATION INSENSITIVE 3 (VIN3), is necessary for the modifications to FLC and FLM chromatin that are associated with an epigenetically silenced state and with acquisition of competence to flower. In addition, VIL1 regulates FLM independently of VIN3 in a photoperiod-dependent manner.Supplemental material is available at http://www.genesdev.org.Received September 13, 2006; revised version accepted October 13, 2006. The transition to flowering is a critical developmental event in the plant life cycle. In many plants, the perception of seasonal changes affects the timing of this transition. Two environmental cues that many plant species monitor for flowering time control are the prolonged cold of winter and changing day length; these cues promote flowering through the vernalization and photoperiod pathways, respectively. Most accessions of Arabidopsis thaliana exhibit a facultative response to these signals: In the absence of either environmental cue, flowering is delayed but nevertheless eventually occurs.In Arabidopsis, vernalization results in the mitotically stable repression of the potent floral repressor, FLOW-ERING LOCUS C (FLC) (Michaels and Amasino 1999;Sheldon et al. 1999). Vernalization-mediated repression of FLC is associated with histone modifications such as methylation of histone H3 Lys 9 (H3K9) and Lys 27 (H3K27) as well as H3 deacetylation (Bastow et al. 2004;Sung and Amasino 2004). A plant homeodomain (PHD) finger-containing protein, VERNALIZATION , is required for FLC repression by vernalization and the associated modifications to FLC chromatin (Sung and Amasino 2004). Here we show that a related PHD finger-containing protein, VIN3-LIKE 1 (VIL1), identified in a screen for proteins that interact with VIN3, cooperates with VIN3 in the vernalizationmediated repression of FLC. Furthermore, independently of VIN3 activity, VIL1 mediates the photoperiod-specific repression of another member of the FLC clade. Thus, VIL1 is involved in the regulation of flowering by two environmental-sensing pathways. Results and DiscussionBecause VIN3 is essential for the vernalization response (Sung and Amasino 2004) and PHD finger-containing proteins are often members of multisubunit chromatin remodeling complexes (Bienz 2006), we searched for potential components of a VIN3 complex using the yeast two-hybrid system. This screen revealed two independent VIN3-interacting clones encoding C-terminal regions of At3g24440. In...
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