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First published online September 15, 2009; 10.1104/pp.109.145581 Plant Physiology 151:1688-1697 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
A Single Amino Acid Change in the Enhancer of Zeste Ortholog CURLY LEAF Results in Vernalization-Independent, Rapid Flowering in Arabidopsis1,[C],[W],[OA]Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53706–1544
Many strains of Arabidopsis (Arabidopsis thaliana) require exposure to prolonged cold for rapid flowering, a process known as vernalization. Vernalization in Arabidopsis results in the suppression of FLOWERING LOCUS C (FLC), a repressor of flowering. In a screen for mutants that no longer require vernalization for rapid flowering, we identified a dominant allele of the Enhancer of Zeste E(z) ortholog CURLY LEAF (CLF), clf-59. CLF is a Polycomb Group gene, and the clf-59 mutant protein contains a proline-to-serine transition in a cysteine-rich region that precedes the SET domain. Mutant plants are early flowering and have reduced FLC expression, but, unlike clf loss-of-function mutants, clf-59 mutants do not display additional pleiotropic phenotypes. clf-59 mutants have elevated levels of trimethylation on lysine 27 of histone H3 (H3K27me3) at FLC. Thus, clf-59 appears to be a gain-of-function allele, and this allele represses FLC without some of the components required for vernalization-mediated repression. In the course of this work, we also identified a marked difference in H3K27me3 levels at FLC between plants that contain and those that lack the FRIGIDA (FRI) gene. Furthermore, FRI appears to affect CLF occupancy at FLC; thus, our work provides insight into the molecular role that FRI plays in delaying the onset of flowering.
The switch from vegetative to reproductive growth is an important developmental transition in the life history of flowering plants. The proper timing of this switch is critical for reproductive success, especially in temperate climates where flower and seed production often needs to align with favorable weather conditions and/or the presence of pollinators. To ensure that flowering occurs at an optimal time of the year, plants have evolved mechanisms to sense and respond to seasonal environmental cues. One such cue is the prolonged cold of winter. The promotion of flowering by cold occurs through a process known as vernalization (for review, see Sung and Amasino, 2005  ; Dennis and Peacock, 2007).
Among accessions of Arabidopsis (Arabidopsis thaliana), there is variation in the requirement for vernalization. In winter-annual accessions, flowering is delayed unless plants undergo vernalization; summer-annual accessions do not require prolonged cold for rapid flowering. Natural variation at two loci in Arabidopsis, FRIGIDA (FRI) and FLOWERING LOCUS C (FLC), has a major influence on the requirement for vernalization (Napp-Zinn, 1979
Arabidopsis also contains a group of genes known collectively as the autonomous pathway that, in contrast to FRI, act as repressors of FLC. LUMINIDEPENDENS (LD), FCA, FLOWERING LOCUS D (FLD), and FVE are among this group of genes (Lee et al., 1994b
Chromatin modification appears to play a large role in setting the expression level of FLC. In genetic backgrounds that favor elevated FLC expression, active chromatin modifications accumulate at FLC, and several proteins required for the deposition of these modifications have been identified (for review, see Schmitz and Amasino, 2007
The Arabidopsis protein CURLY LEAF (CLF) is an ortholog of the Drosophila PRC2 component Enhancer of Zeste [E(z)], a methyltransferase with specificity for H3K27 (Goodrich et al., 1997 Here, we describe a gain-of-function allele of CLF that was isolated in a screen for suppressors of delayed flowering in an autonomous pathway mutant background. This allele leads to elevated H3K27me3 at FLC chromatin, FLC mRNA repression, and rapid flowering in backgrounds that would otherwise require vernalization. In addition, we also demonstrate that the presence of FRI has a substantial effect on the degree of H3K27me3 accumulation and CLF occupancy at FLC.
A Mutation in CLF Suppresses FLC-Mediated Delayed Flowering via Reduced FLC Expression
Mutants with lesions in the autonomous pathway gene LD are delayed in flowering due to elevated expression of FLC (Michaels and Amasino, 2001
Mutations in autonomous pathway genes lead to delayed flowering via elevated expression of FLC (Michaels and Amasino, 2001 ). Similarly, plants carrying a functional copy of FRI also display FLC-dependent late flowering (Koornneef et al., 1994; Lee et al., 1994a; Michaels and Amasino, 1999; Sheldon et al., 1999). To evaluate whether the effect on flowering was specific to ld, clf-59 was combined genetically with fca, another autonomous pathway mutant (MacKnight et al., 1997), and a Col line that contains a functional copy of FRI (FRI-Col; Lee et al., 1994a); in both cases, clf-59 suppressed late flowering in a semidominant manner (Fig. 1C). Rapid flowering was also observed when clf-59 was introduced transgenically into the autonomous pathway mutants fld (He et al., 2003) and fve (Ausin et al., 2004; Fig. 1D). Because autonomous pathway mutants and FRI-containing plants are delayed in flowering due to elevated FLC levels (Michaels and Amasino, 2001), rapid flowering in a clf-59 background could result from FLC repression. Indeed, ld-3, fca-1, and FRI-Col all displayed reduced levels of FLC mRNA when combined with clf-59 (Fig. 1E). Thus, rapid flowering in clf-59 results, at least in part, from decreased expression of FLC.
The CLF protein contains several conserved motifs (Fig. 2
). The C5 motif functions in protein-protein interactions (Chanvivattana et al., 2004
In addition to CLF, Arabidopsis contains two additional E(z)-like genes, SWINGER (SWN) and MEDEA (MEA; Grossniklaus et al., 1998 ; Chanvivattana et al., 2004). MEA is essential for endosperm development (Grossniklaus et al., 1998). SWN is partially redundant in function with both CLF and MEA (Chanvivattana et al., 2004; Wang et al., 2006). For example, CLF and SWN act redundantly in the silencing of FLC as a result of vernalization. Both clf and swn single mutants can become vernalized, but down-regulation of both genes simultaneously results in vernalization insensitivity (Wood et al., 2006). Given the pronounced effect of clf-59, it was of interest to determine whether the P-to-S substitution in SWN and MEA would also cause rapid flowering or possibly other developmental aberrations. Accordingly, this substitution was introduced into genomic clones of both SWN and MEA. The mutant genes were subsequently transformed into Col and FRI-Col backgrounds. All transgenic plants flowered synchronously with the nontransformed parents (data not shown). Thus, the P-to-S transition in MEA and SWN does not cause enhanced FLC repression. In addition, no visual phenotypic differences were observed in plants containing modified SWN or MEA at any stage of development. Possible reasons for lack of a phenotype in plants with modified SWN or MEA include, but are not limited to, wild-type CLF masking an effect of these modified transgenes or simply the lack of an effect of this substitution on SWN or MEA activity. As noted below, the only effect of the P-to-S transition in clf-59 that we observe is on flowering and FLC expression.
Loss-of-function mutations in clf cause a number of phenotypes, including upward curling of leaves and abnormal flower development (Goodrich et al., 1997
The effect of a clf loss-of-function allele, clf-28, on flowering time and FLC expression was also examined. clf-28 hastened flowering in FRI-Col but to a much lesser degree than clf-59 (Fig. 4A ) and, unlike clf-59, did not have a significant effect on FLC expression (Fig. 4B). This distinction indicates that clf-59 is a gain-of-function allele with respect to FLC expression as opposed to a dominant negative.
In the absence of FRI, clf-28 also hastened flowering despite slightly elevated FLC levels (Fig. 4, A and B). Such FLC derepression in a loss-of-function clf mutant has been reported previously (Jiang et al., 2008 ). Early flowering in clf loss-of-function mutants likely results from derepression of FT (Jiang et al., 2008), a strong promoter of flowering that when overexpressed bypasses the repressive effects of FLC (Michaels et al., 2005).
CLF catalyzes the methylation of H3K27. Previous studies have extensively examined the distribution of H3K27me3 across FLC and surrounding chromatin (Bastow et al., 2004
When assaying H3K27me3 in clf-59 plants, a marked difference in H3K27me3 levels was observed between Col and FRI-Col (Fig. 5, A and B). To our knowledge, this is the first report of the effect of FRI on H3K27 methylation. Reduced H3K27me3 levels in the presence of FRI indicate that, in a genetic sense, FRI is a negative regulator of H3K27me3 at FLC. Moreover, autonomous pathway mutants also display reduced levels of H3K27me3 at FLC, which are comparable to levels seen in FRI-Col (Fig. 5, C and D). Thus, in backgrounds that lack FRI, the autonomous pathway is required for the elevated H3K27me3 levels found at FLC.
Given the elevated levels of H3K27me3 in Col relative to FRI-Col in nonvernalized plants, it was of interest to determine whether vernalization simply elevates H3K27me3 levels to those found in Col or if additional H3K27me3 accumulates in Col upon exposure to prolonged cold. H3K27me3 levels are in fact elevated in Col following cold treatment; however, the fold change is not as great as that seen in a FRI-Col background (Fig. 5E). In both vernalized and nonvernalized plants, FLC had higher levels of H3K27me3 in Col than in FRI-Col. However, it should be noted that the 30-d cold treatment given in these experiments is not saturating with respect to the acceleration of flowering (Lee and Amasino, 1995
In addition to CLF, several other genes have been shown to play a role in the vernalization-mediated deposition and maintenance of H3K27me3 at FLC. These include the PcG gene VERNALIZATION2 (VRN2; Gendall et al., 2001
Although the loss of vil1 did not affect the ability of clf-59 to repress FLC and cause early flowering (Fig. 6C), FRI vil1 clf-59 plants did display several pleiotropic phenotypes, including pale green leaves and downward leaf curling (Fig. 6, D and E), the opposite of that seen in clf loss-of-function mutants. Thus, VIL1 appears to be required for wild-type leaf morphology in the presence of clf-59.
As discussed above, FRI-Col and autonomous pathway mutants have relatively low levels of H3K27me3 at FLC chromatin when compared to Col (Fig. 5). In addition, it has been shown that clf loss-of-function mutants have reduced H3K27me3 levels at FLC chromatin in a Col background (Jiang et al., 2008
GFP:CLF was also introduced into fca-9 and fld-3 backgrounds. In both cases, the autonomous pathway mutant displayed lower levels of CLF occupancy at FLC chromatin relative to the wild type (Fig. 7B). Thus, as with FRI, the fca and fld genetic backgrounds create a condition that leads to reduced occupancy of CLF protein at FLC chromatin. We also examined the effect of prolonged cold on the enrichment of CLF at FLC. After a 35-d cold exposure, a difference in CLF occupancy at FLC could no longer be detected between plants that contain and those that lack FRI (Fig. 7C). This 35-d cold exposure was sufficient to substantially hasten flowering time in FRI-Ws (Fig. 7D). Thus, with vernalization, the presence of FRI no longer affects the amount of CLF that occupies FLC chromatin, and increased CLF occupancy at FLC after prolonged cold correlates with the vernalization-mediated increase in H3K27me3 at FLC.
We have identified a gain-of-function allele of CLF, clf-59, that reduces the level of FLC expression and thus eliminates the requirement for vernalization in winter-annual types of Arabidopsis. CLF is a PcG protein that functions in a complex, PRC2, which has conserved features in plants and animals. Plant genomes typically contain multiple copies of conserved PRC2 components [for example, Arabidopsis has three E(z) homologs: CLF, SWN, and MEA], and these components interact with members of the plant-specific, VIN3-like family of proteins (Wood et al., 2006 ; De Lucia et al., 2008). Thus, there is potential for much variability in the specific PcG complexes that assemble in plants. The clf-59 protein may either enhance the activity of a particular PcG complex or allow for the formation of a novel PcG complex that possesses high affinity for FLC chromatin.
clf-59 harbors a Pro-to-Ser amino acid transition in a Cys-rich region. Although the specific biochemical role of this region is not known, it contains two contiguous domains with a unique spacing of Cys residues called CXC domains as first described in ENX-1, the human homolog of E(z) (Hobert et al., 1996
Both clf-59 and clf loss-of-function alleles hasten the onset of flowering; however, the two types of alleles do so via different mechanisms. clf-59 causes hyperrepression of FLC expression with no noticeable effect on AG. In contrast, clf loss-of function mutants cause derepression of several genes, including AG, FLC, and FT (Goodrich et al., 1997
It is interesting to compare the degree of FLC derepression that we observe in a clf loss-of-function mutant to that reported previously (Jiang et al., 2008
The wild-type function of the autonomous pathway is to repress FLC expression (Michaels and Amasino, 2001
In this work, we present data that are consistent with FRI playing an antagonistic role with respect to PcG occupancy at FLC. We observe that H3K27me3 levels, a mark deposited by PcG protein complexes, were less abundant at FLC chromatin in a FRI-Col background relative to Col. We provide a possible explanation for the difference in H3K27me3 levels in the presence or absence of FRI by demonstrating that CLF, a PcG protein that catalyzes H3K27me3 deposition, is less abundant at FLC in FRI-Col relative to Col plants. Because CLF occupancy at FLC is reduced in a FRI background, one might expect a clf loss-of-function mutant to have less of an effect on FLC expression in a FRI-Col background; indeed, this is consistent with the lack of FLC derepression we observe in FRI clf plants. A molecular signature present in vernalized Arabidopsis plants is the accumulation of H3K27me3 at FLC (Schubert et al., 2006
Chromatin modification has been shown in many systems to reinforce and/or maintain states of gene expression. Much of the data presented here and in other articles on FLC chromatin and flowering show correlations between the transcriptional level of FLC and particular chromatin modifications. We show, for example, that levels of H3K27me3, a repressive chromatin mark, and occupancy of CLF, a PcG protein, are decreased at FLC in two genetic situations in which FLC expression is elevated: the presence of FRI and the lack of autonomous pathway genes. The differential accumulation of marks such as H3K27me3 at FLC may very well be an indirect consequence of the effect that FRI and autonomous pathway genes have on FLC transcription. Indeed, just as we show that FRI leads to a reduction in CLF occupancy at FLC, a recent report has shown that FRI also correlates with the accumulation of a COMPASS complex component at FLC that modifies chromatin to an active state (Jiang et al., 2009 The unique gain-of-function clf-59 allele results in an increase in the abundance of H3K27me3 at FLC in the presence of FRI. Thus, the clf-59 protein might be immune to the ability of FRI or loss of autonomous pathway components to reduce CLF occupancy at FLC chromatin in the absence of vernalization; thus, clf-59 may be able to accumulate to higher levels than wild-type CLF at FLC in these genetic backgrounds. Alternatively, clf-59 may produce a hyperactive protein that can elevate H3K27me3 levels without increased occupancy at FLC. It is intriguing that clf-59 can suppress FLC expression in nonvernalized plants to a level comparable to that found in the wild type after vernalization in the absence of proteins known to mediate the vernalization-induced silencing of FLC, including VRN2, VIN3, and VIL1. Future studies addressing the unique biochemical properties of the clf-59 protein may further our knowledge of FLC regulation and PcG targeting in general by providing a better understanding of the molecular events that either recruit or exclude PcG genes to FLC chromatin.
Plant Growth Conditions and Mutant Stocks
Plants were grown under cool-white fluorescent lights at 22°C in long-day photoperiods (16 h light: 8 h dark). Cold treatments were carried out at 4°C under cool-white fluorescent lights. The clf-59 mapping population was created by crossing ld-1 to ld-3 clf-59. The ld-1 and ld-3 mutants are from the Col and Ws-2 backgrounds, respectively (Lee et al., 1994b
Tissue was harvested from 7-d-old seedlings. RNA was isolated using TRI reagent (Sigma-Aldrich). For northern analysis, 12 µg of total RNA was run on a 1% agarose denaturing formaldehyde gel and transferred to a nylon filter (Hybond). A DNA probe was used that was complementary to the 3' untranslated region of FLC. Real-time PCR was performed with the 7000 Real-Time PCR System (Applied Biosystems) using the DyNAmo Flash SYBR Green qPCR Kit (Finnzymes). The PCR parameters were as follows: one cycle of 15 min at 95°C, 40 cycles of 15 s at 95°C, 20 s at 58°C, and 45 s at 72°C. The constitutively expressed gene encoding the A3 subunit of protein phosphatase 2A was used as a control (Czechowski et al., 2005
Tissue was harvested from 7-d-old seedlings. Chromatin samples were prepared as described (Gendrel et al., 2005 Sequence data from this article can be found in the Arabidopsis Genome Initiative database under the following accession numbers: CLF, At2g23380; FLC, At5g10140; FRI, At4g00650; LD, At4g02560; FCA, At4g16280; FLD, At3g10390; FPA, At2g43410; FVE, At2g19520; AG, At4g18960; VIL1, At3g24440; VRN2, At4g16845; VIN3, At5g57380; VRN1, At3g18990; MEA, At1g02580; and SWN, At4g02020.
The following materials are available in the online version of this article.
We thank Dr. Scott Michaels for identifying the clf-59 mutant and for helpful discussions. We also thank Drs. Justin Goodrich and Daniel Schubert for supplying constructs and seed used in this work and the Salk Institute Genomic Analysis Laboratory for providing the Arabidopsis T-DNA insertion lines. Received August 3, 2009; accepted September 8, 2009; published September 15, 2009.
1 This work was supported by the University of Wisconsin, the National Institutes of Health (grant no. 1R01GM079525), and the National Science Foundation (grant no. 0446440).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Richard M. Amasino (amasino{at}biochem.wisc.edu).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.109.145581 * Corresponding author; e-mail amasino{at}biochem.wisc.edu.
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