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First published online February 9, 2007; 10.1104/pp.107.095521 Plant Physiology 143:1660-1668 (2007) © 2007 American Society of Plant Biologists OPEN ACCESS ARTICLE
Involvement of the Histone Acetyltransferase AtHAC1 in the Regulation of Flowering Time via Repression of FLOWERING LOCUS C in Arabidopsis1,[W],[OA]State Key Laboratory of Plant Genomics and Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China 100101 (W.D., C.L., Y.P., X.D., L.N., X.C.); Graduate School, Chinese Academy of Sciences, Beijing, China 100039 (W.D., L.N.); and College of Life Science and Technology, Shanxi University, Taiyuan, China 030006 (Y.P.)
Histone acetylation is an important posttranslational modification correlated with gene activation. In Arabidopsis (Arabidopsis thaliana), the histone acetyltransferase AtHAC1 is homologous to animal p300/CREB (cAMP-responsive element-binding protein)-binding proteins, which are the main histone acetyltransferases participating in many physiological processes, including proliferation, differentiation, and apoptosis. The functions of p300/CREB-binding proteins in animals are well characterized, whereas little is known about the roles of AtHAC1 in developmental control in Arabidopsis. Lesions in AtHAC1 caused pleiotropic developmental defects, including delayed flowering, a shortened primary root, and partially reduced fertility. Analysis of the molecular basis of late flowering in hac1 mutants showed that the hac1 plants respond normally to day length, gibberellic acid treatment, and vernalization. Furthermore, the expression level of the flowering repressor FLOWERING LOCUS C (FLC) is increased in hac1 mutants, indicating that the late-flowering phenotype of hac1 mutants is mediated by FLC. Since histone acetylation is usually associated with the activation of gene expression, histone modifications of FLC chromatin are not affected by mutations in HAC1 and expression levels of all known autonomous pathway genes are unchanged in hac1 plants, we propose that HAC1 affects flowering time by epigenetic modification of factors upstream of FLC.
Posttranslational modifications of histone N termini play fundamental roles in maintaining chromatin structure and function. One such modification, histone acetylation, has been implicated in many biological processes. In humans, histone acetylation is catalyzed by distinct histone acetyltransferase (HAT) families including the p300/CREB (cAMP-responsive element-binding protein)-binding protein (CBP) family, the TAFII-250 family, the MYST (MOZ, Ybf2/Sas3, Sas2, and Tip60) family, and the GNAT (GCN5-related N-terminal acetyltransferase) family. The p300/CBP family plays a major role in transcriptional regulation by promoting acetylation of both histones and nonhistone proteins, such as the transcription factors CREB, p53, HIV-1 Tat protein, and Stat3 (Sterner and Berger, 2000  ; Liu et al., 2004). Therefore, p300/CBP are not only HATs, but also factor acetyltransferases, and both types of activity are physiologically important for p300/CBP functions (Sterner and Berger, 2000). In addition, because of their transcriptional coactivator functions, p300/CBP are proposed to contribute to transcriptional activation by directly interacting with DNA-binding transcription factors and/or being part of coactivation complexes (Dai et al., 1996; Goldman et al., 1997; Seo et al., 2001). In general, the histone acetylation status of a gene correlates with its transcriptional activity (Cheung et al., 2000; Strahl and Allis, 2000).
The p300/CBP family exists in most multicellular eukaryotes, including mammals, Drosophila melanogaster, and Arabidopsis (Arabidopsis thaliana; Sterner and Berger, 2000
In Arabidopsis, there are five p300/CBP HAT homologs, named AtHAC1 (or PCAT2), AtHAC2 (or PCAT1), AtHAC4 (or PCAT3), AtHAC5 (or PCAT4), and AtHAC12 (Bordoli et al., 2001 In this study, we isolated Arabidopsis mutants with T-DNA insertions in the HAC1 gene and investigated their effects on plant development. We showed here that HAC1 played an important role in vegetative and reproductive development, and lesions in HAC1 caused a late-flowering phenotype in Arabidopsis. hac1 mutants responded normally to day length, gibberellin (GA), and vernalization treatments, and displayed an increased level of transcripts of FLOWERING LOCUS C (FLC) and two additional MADS-box genes, MADS AFFECTING FLOWERING 4 (MAF4) and MAF5. Therefore, HAC1 is critical for the normal regulation of flowering time in Arabidopsis.
Isolation and Molecular Characterization of hac1 Mutants To investigate the roles of the CBP homologs in Arabidopsis (AtHAC1, AtHAC2, AtHAC4, AtHAC5, and AtHAC12), T-DNA insertion mutants from the SALK or GABI-Kat collection were screened for homozygotes. No obvious developmental defects were observed from single mutants of hac2, hac4, hac5, or hac12 under normal growth conditions. However, three different T-DNA insertions in HAC1 (named hac1-3 for SALK_080380, hac1-4 for SALK_082118, and hac1-5 for GABI-314B12) showed a late-flowering phenotype. Therefore, we focused our investigations on the functions of HAC1 gene.
The HAC1 gene contains 17 exons and encodes a 1,691 amino acid polypeptide with distinct domains including two ZZ-type and two TAZ-type zinc finger domains (Fig. 1, A and B
). These domains have been shown in other organisms to mediate protein-protein interactions with transcription factors (Ponting et al., 1996
RNA-blot analysis was performed to confirm the efficient disruption of HAC1 mRNA in hac1 plants. When full-length coding sequence (CDS) of HAC1 was used as a probe, we did not detect the full-length transcript of HAC1 in hac1 mutants. However, a short transcript was observed in both hac1-3 and hac1-4 plants, indicating that neither hac1-3 nor hac1-4 was a null allele (Fig. 1C). Because the main functional domains of HAC1 were located in the C terminus, we performed RNA-blot analysis using a probe specific to the C-terminal portion of the HAC1 gene (Fig. 1B) and no mRNA containing these conserved domains could be detected (Fig. 1D). Thus, our mutant alleles are unlikely to produce any functional protein. A backcross between the hac1 homozygote and a wild-type line resulted in wild-type phenotype in F1 plants. The self-pollinated F1 progeny displayed an approximately 3:1 ratio of wild-type and hac1 phenotype, indicating that hac1 is a recessive, single-gene mutation. In addition, different alleles of hac1 (hac1-3, hac1-4, and hac1-5) do not complement each other. For example, the hac1-3/hac1-4 trans-heterozygous F1 plants from a cross between homozygous hac1-3 and hac1-4 showed the same phenotype as hac1-3 and hac1-4 plants (Fig. 2, E and F ), and no segregation was observed in the F2 progeny (data not shown). These data indicate that the hac1 mutant is recessive and the observed phenotypes of hac1 mutants are indeed caused by disrupting HAC1 activity.
The hac1 Mutants Display Pleiotropic Developmental Defects in Arabidopsis In addition to the late-flowering phenotype, we examined other developmental defects in hac1 plants. The primary roots of hac1 mutants were shorter than those of the wild-type plants when measured after 6 d of growth (Fig. 2A). The hac1 mutants also had reduced fertility in the first few siliques (Fig. 2, B and C). In the partial sterile flowers, the pollen produced by hac1 mutants didn't reach the stigmas due to the short stamens resulting in the reduction of pollination and fertility (data not shown). The first 1 to 4 siliques of hac1 were about 30% shorter than those of wild-type plants. Siliques 5 to 8 were longer than the first 1 to 4, but still shorter than those of wild type (Fig. 2C). Siliques formed after these were similar to those of wild-type plants.
The most notable phenotype of hac1 plants is late flowering (Fig. 2, D–G). In Arabidopsis, flowering time is regulated by four major pathways, namely the photoperiod, GA, vernalization, and autonomous pathways (Simpson et al., 1999
The growth regulator GA promotes flowering of Arabidopsis. Exogenous application of GA accelerates flowering in wild-type Arabidopsis, particularly under SD (Wilson et al., 1992
Vernalization is a process by which flowering is promoted by prolonged exposure to the cold of a typical winter. Mutants in the vernalization pathway no longer respond to prolonged cold to promote flowering (Gendall et al., 2001 ; Amasino, 2004; Bastow et al., 2004; Sung and Amasino, 2004b; Amasino, 2005; Kim et al., 2005; Sung and Amasino, 2005). To determine whether vernalization could reverse the late-flowering phenotype of hac1, the hac1 mutants and wild-type plants were grown at 4°C for 6 or 10 weeks before transferring to 23°C under LD. Similar to the wild-type plants, the hac1 mutants flowered much earlier after vernalization treatment (Fig. 3B). After vernalization for 10 weeks, hac1 mutants and wild-type plants flowered almost at the same time (Fig. 3B). Therefore, the hac1 lesions do not affect the vernalization pathway.
The autonomous and vernalization pathways converge on FLC, a MADS-box transcription factor, which is a central regulator of floral transition in Arabidopsis (Michaels and Amasino, 1999 Since hac1 mutants are late flowering under both LD and SD, GA and vernalization treatments reverse the late-flowering phenotype, and hac1 mutants have an increased level of FLC mRNA, HAC1 behaves as a member of the autonomous pathway.
The components of the autonomous pathway, including FCA (Macknight et al., 1997
To determine whether the late-flowering phenotype of hac1 plants was solely due to the increase of FLC expression, hac1 mutants were crossed with an flc null allele, flc-3 (Michaels and Amasino, 1999
Epigenetic modifications have been shown to play an essential role in regulating FLC expression. Two components of the autonomous pathway, FLD and FVE, negatively regulate FLC by participating in the deacetylation of chromatin (He et al., 2003 ; Ausin et al., 2004; Kim et al., 2004). The vernalization pathway also regulates FLC expression by chromatin acetylation and methylation (Bastow et al., 2004; Finnegan et al., 2004; He et al., 2004; Sung and Amasino, 2004a, 2004b; Amasino, 2005; He and Amasino, 2005). Furthermore, REF6, which encodes a nuclear protein with jumonji and zinc finger domains, represses FLC transcription through histone deacetylation (Noh et al., 2004). Thus, histone acetylation is an essential modification of FLC chromatin.
Although it is clear that histone acetylation/deacetylation regulates FLC expression, the identity of the HAT responsible for this process is unknown. To investigate whether HAC1 acetylates histones at FLC, we performed chromatin immunoprecipitation assays using 12-d-old seedlings of hac1 mutant and wild-type plants. In addition to histone acetylation, di- and trimethylation of H3K4, which are hallmarks for active chromatin, were also analyzed (Bernstein et al., 2002
Histone acetylation is known to regulate flowering time in Arabidopsis (Tian and Chen, 2001 ; He et al., 2003; Ausin et al., 2004; Tian et al., 2005). However, the HATs involved have not been identified. Our studies provide a link between a HAT, HAC1, and flowering-time control in Arabidopsis. The late-flowering phenotype of hac1 mutants was FLC dependent. First, hac1 plants flowered later than Col under LD and SD, which is a characteristic of FLC repressing flowering (Fig. 2, D–G). Second, hac1 mutants had a proper vernalization response that promotes flowering by repressing the expression of FLC (Fig. 3B). Third, the late-flowering phenotype of hac1 mutants was suppressed by an flc null mutant (Fig. 5). Finally, the mRNA levels of FLC were increased in hac1 mutants (Fig. 4A). In addition to the increase of FLC expression, a portion of the late-flowering phenotype of hac1 mutants could be due to other floral repressors because the flowering time of hac1/flc-3 double-mutant plants was still slightly later than that of flc-3 under LD (Fig. 5). Consistent with this hypothesis, the expression of two additional MADS-box genes in the FLC clade, MAF4 and MAF5, were also up-regulated in hac1 mutants (Fig. 4B). However, the up-regulation of MAF4 and MAF5 was not unique in hac1 mutants because some autonomous pathway mutants also resulted in increased expression of MAF4 and MAF5 (Supplemental Fig. S2).
In addition to the late-flowering phenotypes, mutations in HAC1 caused pleiotropic developmental defects, including shortened primary roots and partially reduced fertility. These pleiotropic effects observed in hac1 may be caused by loss of acetylation at multiple target genes, similar to mutations in other genes responsible for chromatin modifications. The Arabidopsis genome encodes five HACs, whereas the number of p300/CBP proteins in animals is only one to two (Pandey et al., 2002
In humans, the transcriptional regulation by p300/CBP appears to be exerted through multiple mechanisms. p300/CBP have been shown to acetylate both nucleosomal histones and certain sequence-specific transcription factors, leading to transcriptional activation in most cases (Sterner and Berger, 2000 In general, histone acetylation correlates with gene activation and when HAC1 is disrupted, one would expect that the expression of its direct target genes would be reduced. In hac1 mutants, the expression levels of FLC, MAF4, and MAF5 are increased (Fig. 4, A and B). Therefore, FLC, MAF4, and MAF5 may not be the direct targets of HAC1. Instead, HAC1 might regulate the expression of a trans-acting repressor of FLC, MAF4, and MAF5. Since the vernalization and autonomous pathway genes repress the expression of FLC, and vernalization rescues the late-flowering phenotype of hac1 mutants, it is unlikely that the targets of HAC1 are in the vernalization pathway. Therefore, we examined the mRNA expression of all known autonomous pathway genes by RT-PCR and real-time PCR, but did not find any significant differences in hac1 plants (Fig. 4C). One possible explanation is that HAC1 acetylates the histones of an unknown component that represses FLC and/or MAF4/5. Alternatively, HAC1 might acetylate a known or an unknown component of the autonomous pathway to affect its activity at posttranslational level. A third possibility is that the direct target of HAC1 (or HAC1 itself) might be involved in the recruitment of the known or unknown autonomous pathway components to FLC chromatin. Further studies aimed at identifying the direct targets of HAC1 in the FLC-dependent pathway would help to distinguish between these possibilities.
Plant Materials and Growth Conditions All the Arabidopsis (Arabidopsis thaliana) lines used in this study were in ecotype Col-0. Plants were grown at 23°C ± 1°C. The photoperiods for LD were 16 h of light followed by 8 h of darkness and 8 h of light followed by 16 h of darkness for SD. For flowering-time measurements, plants were sowed side by side and transferred into Versatile Environmental Test Chamber (MLR-350H, SANYO) at 23°C ± 1°C. Flowering time was measured by counting the total number of rosette and cauline leaves at flowering and the days from germination to floral bud formation. For GA treatment, plants were grown on soil under SD, and a GA solution of 100 µM was sprayed once a week until flowering. Ethanol was sprayed as untreated control. For vernalization treatment, the hac1 mutants and wild-type plants were grown side by side at 4°C for 6 or 10 weeks under SD and then transferred to 23°C under LD. Nonvernalized control seeds were grown for 3 d under vernalization conditions.
DNA was isolated from hac1-3, hac1-4, and hac1-5 mutants. T-DNA border primers cx0101 LBb1 or cx0102 LBa1 were used to amplify DNA from mutants obtained from the SALK collection and T-DNA border primer cx1475 was used for GABI T-DNA insertion mutant hac1-5. The gene-specific primers were cx0517 and cx0516 for hac1-3 and cx0515 and cx0514 for hac1-4. hac1-5 was amplified with cx0514 and cx0517. Primer sequences were listed in Supplemental Table S1.
Seeds of Col-0 and hac1 mutants were surface sterilized with 10% bleach for 15 min, washed with sterile water, and plated on 9 x 9-cm2 dishes containing 30 mL of agar-solidified culture medium. This medium contains 1x Murashige and Skoog basal medium with vitamins (PhytoTechnology Laboratories) supplemented with 3% Suc and 0.8% to 1% plant tissue culture agar. The plates were kept at 4°C for 3 d and then placed vertically to allow the downward growth of roots in a growth chamber under LD at 23°C. After 6 d, measurements of primary root length were made for each sample.
Transcript levels were measured either by real-time PCR and RT-PCR or by RNA gel blots. Total RNA extraction and RT-PCR were performed as previously described by Liu et al. (2005)
For RNA gel-blot analysis, RNA was transferred onto N+ nylon membrane and probed with [
The chromatin immunoprecipitation experiments were performed as described by Johnson et al. (2002)
The following materials are available in the online version of this article.
We thank Dr. R. Jorgensen for analysis of the HAC1 protein structure, Dr. L. Johnson for critical reading and comments on the manuscript, and Dr. R. Amasino for providing flc-3 seeds. We also thank the Arabidopsis Biological Resources Center at The Ohio State University and Bernd Weisshaar for providing SALK and GABI T-DNA insertion lines in the Col background. Received January 5, 2007; accepted January 31, 2007; published February 9, 2007.
1 This work was supported by National Basic Research Program of China (grant no. 2005CB522400 to X.C.), by National Natural Science Foundation of China (grant no. 30571032 to C.L., and nos. 30325015, 30430410, and 30621001 to X.C.), and by the Chinese Academy of Sciences (grant no. CXTD–S2005–2). 
2 These authors contributed equally to the paper. 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: XiaoFeng Cao (xfcao{at}genetics.ac.cn).
[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.107.095521 * Corresponding author; e-mail xfcao{at}genetics.ac.cn; fax 86–10–64873428.
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ABSTRACT
RESULTS
CT corresponds to the ratio of each gene expression versus UBQ.
-32P]dCTP-labeled FLC full-length CDS fragment (NM_121052, from 110–700 bp), or HAC1 full-length CDS (NM_106550, from 1–5,076 bp) or C-terminal fragments from 1,873 to 5,076 bp, respectively. Blots were also probed with an Actin probe as a loading control. 
