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First published online December 17, 2008; 10.1104/pp.108.131508 Plant Physiology 149:1196-1204 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Histone H2B Deubiquitination Is Required for Transcriptional Activation of FLOWERING LOCUS C and for Proper Control of Flowering in Arabidopsis1,[C],[W],[OA]Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53706 (R.J.S., Y.T., M.R.D., R.M.A.); and Department of Plant Biology, University of Georgia, Athens, Georgia 30602 (X.Z.)
The spectrum of histone modifications at a given locus is a critical determinant for the correct output of gene expression. In Arabidopsis (Arabidopsis thaliana), many studies have examined the relationship between histone methylation and gene expression, but few studies exist on the relationship between other covalent histone modifications and gene expression. In this work, we describe the role of histone H2B deubiquitination in the activation of gene expression and the consequence of a perturbation of histone H2B deubiquitination in the timing of the floral transition in Arabidopsis. A mutation in a H2B deubiquitinase, UBIQUITIN-SPECIFIC PROTEASE26 (UBP26), results in an early-flowering phenotype. In the ubp26 mutant, mRNA levels of the floral repressor FLOWERING LOCUS C (FLC) and other related family members is decreased. Furthermore, this mutant accumulates H2B monoubiquitination, and has decreased levels of H3K36 trimethylation and increased levels of H3K27 trimethylation at the FLC locus. Thus, UBP26 is required for transcriptional activation of FLC through H2B deubiquitination and is consistent with a model in which deubiquitination is necessary for the accumulation of H3K36 trimethylation and the proper level of transcriptional activation.
Flowering is a highly regulated developmental transition. The perception of both internal and environmental cues ensures that plants transition to flowering during optimal times of the year to maximize their reproductive success. Temperature represents one of the many environmental stimuli that influences flowering. For example, a long exposure to cold, which occurs during winter, enhances the ability to flower in several winter-annual, biennial, or perennial varieties of plants. This acquisition of competence to flower that occurs during a prolonged exposure to cold is known as vernalization (Chouard, 1960  ).
In Arabidopsis (Arabidopsis thaliana), the molecular basis of the vernalization requirement has been well studied. There are both annual (no vernalization requirement) and winter-annual (vernalization-responsive) accessions of Arabidopsis. A study of the genetic basis of the winter-annual habit identified a dominant locus, FRIGIDA (FRI), that confers a vernalization requirement (Napp-Zinn, 1979
FLC expression is strongly repressed by vernalization (Michaels and Amasino, 1999
In Arabidopsis, several genes have been identified as transcriptional activators of FLC and some of its related family members (the FLC family members include FLOWERING LOCUS M [FLM]/MADS AFFECTING FLOWERING1 [MAF1] and MAF2–MAF5, and will be collectively referred to as the FLC clade). Among these activators, EARLY FLOWERING7 (ELF7), UBIQUITIN-CONJUGATING ENZYME1/2 (UBC1/2), HISTONE MONOUBIQUITINATION1/2 (HUB1/2), ARABIDOPSIS TRITHORAX1 (ATX1), and EARLY FLOWERING IN SHORT DAYS/SET DOMAIN GROUP8 have crucial roles in modifying histones at the FLC locus (He et al., 2004
In yeast (Saccharomyces cerevisiae), the Paf1 complex is required for monoubiquitination of histone H2B by the E2 ubiquitin conjugation enzyme Rad6 and the E3 ubiquitin ligase Bre1 (Ng et al., 2003
In efs mutants, expression of FLC is strongly reduced. Furthermore, H3K4me3 is reduced around the transcription start site and H3K36me2/3 is decreased at the promoter and at the first intron of FLC (Kim et al., 2005
Yeast employs two different H2B deubiquitinases, one for gene activation and one for gene silencing (Henry et al., 2003
The Arabidopsis genome contains a family of 27 ubiquitin proteases (UBPs; Yan et al., 2000 In this work, we have studied whether UBP26 also functions in transcriptional activation in Arabidopsis similar to the function of Ubp8 in yeast. Examination of the ubp26-1 mutant revealed an early-flowering phenotype due to decreased expression of FLC and other members of the FLC clade. Furthermore, H2Bub1 was found throughout the coding region of FLC in both wild type and the ubp26-1 mutant. The accumulation of H2Bub1 in ubp26-1 mutants did not affect levels of H3K4me3, but it did affect H3K36me3 and H3K27me3 in FLC chromatin. Collectively, these observations support a role for UBP26 in transcriptional activation of gene expression through H2B deubiquitination, perhaps via an effect on H3K36me3 and H3K27me3.
The ubp26-1 Mutant Displays an Early-Flowering Phenotype The ubp26-1 mutant (in the C24 accession) contains a T-DNA in the fifth exon of UBP26. Reverse transcription (RT)-PCR analysis revealed no expression of the wild-type UBP26 transcript in ubp26-1 plants (Fig. 1, A and B ). ubp26-1 mutants flowered significantly earlier than wild-type C24 in both inductive long days and noninductive short days (Fig. 1, C–E). Consistent with the early-flowering phenotype, the mRNA levels of FLC, MAF2, and MAF3 were quite lower in the ubp26-1 mutant compared to wild type, and the mRNA levels of FLM and MAF4 were also slightly reduced (Fig. 1F). In contrast, the mRNA levels of MAF5 were substantially increased in the ubp26-1 mutant.
In addition to the flowering phenotype, ubp26-1 mutants display a range of other phenotypes such as smaller rosette leaves (Fig. 1, C and D) and weaker apical dominance (only observed after release of secondary inflorescences). To confirm that the ubp26-1 mutation was, in fact, responsible for these phenotypes, we performed complementation experiments. In a subset of the T1 transformant population, all of the ubp26-1 phenotypes were rescued by a transgene containing 2.8 kb of the UBP26 promoter and the entire coding region (Supplemental Fig. S1). Approximately half of the T1 transformants showed severe pleiotropic phenotypes such as multiple vegetative meristems and/or a smaller plant size; these phenotypes were present in both T1 transformants of both the ubp26-1 mutant as well as the wild-type C24 background (Supplemental Fig. S2). Thus, these phenotypes may result from increased UBP26 activity, which indicates that expression of UBP26 in the proper amount and in the appropriate tissues is crucial for normal plant development. Alternatively, these phenotypes could be a result of cosuppression elicited by the transgene.
Many studies of the regulation of the floral transition have been performed in the Columbia (Col) and Landsberg genetic backgrounds. The ubp26-1 allele is in the C24 genetic background. Therefore, we isolated two additional ubp26 mutant alleles in the Col genetic background (ubp26-4 and ubp26-3; Fig. 2A ). However, we were unable to isolate viable plants homozygous for either the ubp26-4 or the ubp26-3 T-DNA allele. We could identify plants hemizygous for the T-DNA, and self-pollination of hemizygous ubp26-4 and/or ubp26-3 plants resulted in an approximately 2:1 ratio of hemizygous:wild type among the progeny. This indicates that the ubp26 lesion results in lethality in the homozygous state and the effect of the mutation is zygotic.
Lethality occurs throughout seed development and occasionally postgermination. Specifically, among the seed derived from self-pollination of plants hemizygous for either ubp26-4 or ubp26-3 we observed a seed abortion rate of approximately 20% (Fig. 2B). Reciprocal crosses between ubp26-4 and wild-type Col demonstrated that the ubp26-4 T-DNA could transmit through either the male or the female gametes. We cleared embryos from seeds produced by plants hemizygous for the ubp26-4 T-DNA to determine if there were specific stages of embryo development that were affected by the ubp26-4 homozygous mutation. From these plants, we observed stochastic arrest throughout embryo development when compared to wild type (Fig. 2, C and D). We were also able to identify seedlings homozygous for ubp26-4 or ubp26-3 (approximately 4%) when segregating populations were sown on nutrient-rich plates, but seedling growth arrested at an early stage, which led to lethality (Fig. 2E). While this work was in progress, Luo et al. (2008) also reported that loss of ubp26 in Col results in a high percentage of lethality. Furthermore, we examined seed from self-pollination of homozygous ubp26-4 plants kindly provided by Liu et al. (2008) and found a high frequency of aborted seeds and seedling lethality with a low frequency of viable plants (Table I
; Supplemental Fig. S3).
None of the viable ubp26-4 homozygous mutant plants that we obtained from seed provided by Liu et al. (2008) displayed an early-flowering phenotype in long days or in short days. Thus, it appears that, in Col, a subset of mutant plants can escape whatever causes embryo and seedling lethality among their siblings, and those that do escape appear to be relatively normal with respect to visible vegetative phenotypes and flowering time. The basis of this difference in flowering and seed viability between Col and C24 ubp26 mutations is currently under investigation.
UBP26 is a UBP that deubiquitinates H2B, and the ubp26-1 mutant has increased levels of H2Bub1 and can lead to a loss of DNA methylation and heterochromatin formation at transgenes (Sridhar et al., 2007
The accumulation of H2Bub1 in ubp26-1 mutants raised the issue of whether other histone modifications might be affected by a change in the status of H2B ubiquitination. We analyzed histone methylation by immunoblot analysis in the same genotypes mentioned above. Lysine 4 trimethylation of histone 3 (H3K4me3) remained unchanged when compared to the respective wild type (Fig. 3). In addition, no changes in Lys 36 methylation of histone 3 (H3K36me) could be observed except in the efs-3 mutants (Fig. 3). In the efs-3 mutant, a decrease in H3K36me3 and an increase in H3K36me1 were observed (Fig. 3). This is consistent with efs-3 functioning as a H3K36 methyltransferase as proposed by Xu et al. (2008) .
H2Bub1 was recently found to accumulate in the transcribed regions of highly expressed genes in humans (Minsky et al., 2008
Mutations in components of the Arabidopsis PAF1 complex severely affect the levels of H3K4me3 at FLC chromatin, although there is no discernable difference in the genome-wide levels of this histone modification (Fig. 3; He et al., 2004 ; Oh et al., 2004, 2008). Therefore, although the accumulation of H2Bub1 had no obvious effect on global levels of H3K4me3, it was of importance to look for local effects of ubp26-1 mutants on H3K4me3 at FLC chromatin. H3K4me3 is a histone modification that facilitates transcription initiation, and as a result it is commonly found around the transcription start site of transcribed genes (Li et al., 2007). ChIP analysis of C24 and ubp26-1 plants revealed a similar spatial distribution of H3K4me3 (Fig. 4C). Furthermore, the amplitude of H3K4me3 variation was similar in wild type and ubp26-1, indicating that perturbation of H2Bub1 did not prevent histone modifications associated with transcription initiation from occurring at FLC chromatin (Fig. 4C).
Although FLC mRNA levels are decreased in the ubp26-1 mutant background the H3K4me3 histone modification typically associated with transcription initiation is present around the transcription start site of FLC. Thus, lower FLC mRNA levels in ubp26-1 might be related to a defect in transcription elongation. In yeast, H2B deubiquitination is linked to H3K36 methylation; H3K36me2/3 is enriched near the 3' end of open reading frames in transcribed genes and is involved in proper transcription elongation of a subset of genes (Li et al., 2007
H3K27me3 Is Highly Enriched at FLC Chromatin in ubp26-1 Mutants
Methylation of H3K27 is a hallmark of repressed genes located in euchromatic regions in Arabidopsis (Zhang et al., 2007
The identification of FLC as a central component in establishing the winter-annual habit has led to a greater understanding of gene activation and gene repression in Arabidopsis. Genetic screens aimed at identifying genes required for FLC activation have revealed three major complexes, the PAF1 complex, the SWR1 complex, and the FRI complex (for review, see Schmitz and Amasino, 2007 ). Paf1 and SWR1 are required, respectively, for transcription initiation of FLC and histone H2A.Z deposition at FLC (Noh and Amasino, 2003; He et al., 2004; Oh et al., 2004; Choi et al., 2005, 2007; Martin-Trillo et al., 2006; Deal et al., 2007; March-Diaz et al., 2007). The FRI complex activates FLC via an undefined molecular mechanism (Johanson et al., 2000; Michaels et al., 2004; Schmitz et al., 2005; Kim et al., 2006; Kim and Michaels, 2006). Recent publications and our work presented in this article have identified H2B monoubiquitination as an additional histone modification required for FLC transcription (Cao et al., 2008; Gu et al., 2009; Xu et al., 2009). To our knowledge, our work is the first report of the role of UBP26, a histone deubiquitinase, in facilitating expression of FLC; UBP26 is likely to act by promoting H3K36me3 and by preventing H3K27me3 at FLC chromatin. The collection of mutants in activators of FLC expression permits exploration into the interplay between different histone modifications. Our studies have demonstrated that accumulation of H2Bub1 at FLC chromatin affects H3K36 methylation, and that H3K4 methylation remains unchanged. This is consistent with a model in which H3K4me3 occurs prior to H2B deubiquitination, whereas H3K36me3 occurs afterward. Our work has also helped to better define the hierarchy of molecular functions required for FLC expression. For example, global levels of H2Bub1 were unaffected in efs-3 mutants, although an increase in levels of H3K36me1 was observed at the expense of H3K36me3 in the ubp26-1 mutant (Fig. 5). These data indicate that EFS functions downstream of H2Bub1 in the methylation of H3K36 and the subsequent activation of gene expression. However, there remains much to learn about the hierarchy of histone modifications at FLC and the molecular role of additional regulators of FLC in this hierarchy. The function of UBP26 in H2B deubiquitination and in gene activation in the regulation of FLC is similar to the function of Ubp8 in yeast. Many of the factors that are involved in the transcriptional activation in yeast are also present in the Arabidopsis genome and play essential roles in FLC activation (Fig. 7 ). This and other work demonstrates that the floral transition and the regulation of FLC provide a good model for investigating the mechanisms of epigenetic gene regulation in plants.
The seed abortion phenotype of the ubp26 mutant is much stronger in Col than in the C24 background (Supplemental Fig. S3; Luo et al., 2008 ). One possibility to account for this variation is that other UBPs can provide UBP activity to permit normal embryo development in C24 but not in Col. Indeed, there are at least 27 UBPs present in the Arabidopsis genome (Yan et al., 2000), and UBP26 does not share the highest degree of amino acid sequence identity to yeast Ubp8 or Ubp10. If the reason for the difference in the seed abortion phenotype is an additional UBP that is active in C24 ubp26 mutants but not in Col ubp26 mutants, a genetic analysis of this difference may identify additional H2B deubiquitinases in Arabidopsis.
Although the role of Ubp8 and UBP26 in transcriptional activation is similar between yeast and Arabidopsis, there are certain differences, at least at well-studied loci. For example, H3K4me3 and H3K36me2 levels at the FLC locus are almost the same in wild type and in ubp26-1 (Figs. 4C and 5B). In contrast, H3K4me3 levels at the yeast GAL1 locus are higher and H3K36me2 levels are lower in the ubp8 mutant compared to wild type (Henry et al., 2003 One proposed function for H3K36 methylation in the body of transcribed genes in yeast is to suppress the initiation of intragenic transcription initiation. We tested for the presence of cryptic transcripts in the body of FLC by RT-PCR analysis using primers located throughout the FLC locus. However, we did not observe evidence of intragenic transcription, as defined by this assay, in efs or ubp26 mutants. Thus, intragenic transcription in the ubp26-1 mutant may not be as prevalent as it is in yeast.
H3K27me3 is a histone modification that is commonly associated with repressed loci located in euchromatin in Arabidopsis. We observed an enrichment of H3K27me3 in the body of FLC in ubp26-1 mutants compared to C24. Thus, the presence of H3K27me3 may provide a mechanism for repressing genes that accumulate H2Bub1. This observation contrasts with recent work that shows that UBP26 is required for maintaining H3K27me3 and repression of PHERES1 (Luo et al., 2008
In conclusion, there are significant parallels in the activation of gene expression in Arabidopsis and yeast. Additional molecular analyses of genes required for transcriptional activation of FLC in Arabidopsis will further refine our knowledge of the interplay between histone modifications and gene expression in both plants and other eukaryotes.
Plant Materials and Growth Conditions
The ubp26-1 mutant was isolated from the C24 background (Sridhar et al., 2007
For the growth condition of plants, we followed the methods described in Schmitz et al. (2008)
The UBP26 genomic clone and its 2.8-kb native promoter were amplified by PCR with Phusion High-Fidelity DNA polymerase (Finnzymes) according to the manufacturer's protocol (the termination codon was not included in the amplification). The T9C5 bacterial artificial chromosome vector, obtained from the Arabidopsis Biological Resource Center, was used as a template for amplification (Choi et al., 1995
Total RNA was isolated using TRIzol reagent (Invitrogen) according to the manufacturer's instructions. First-strand cDNA synthesis was performed on 2 µg of RNA using the M-MLV system for RT-PCR (Promega) followed by PCR amplification with ExTaq DNA polymerase (Takara Mirus) according to the manufacturer's recommendations. Primers used to amplify the cDNAs and PCR conditions are listed in Supplemental Table S1. PCR products were separated on a 2.5% agarose gel. All RT-PCR results presented are representative data of at least two biological replicates.
Nuclear protein extracts were isolated from a chromatin preparation as described in the ChIP protocol in Gendrel et al. (2005)
Tissue was harvested from seedlings 7 d after germination. Chromatin samples were prepared as described (Gendrel et al., 2005
The following materials are available in the online version of this article.
We are grateful to Katsiaryna Frantskevich for technical assistance and to other members of the Amasino Laboratory for helpful discussions. We would like to thank Dr. Jian-Kang Zhu and Dr. Xing-Wang Deng for providing ubp26-1 and ubp26-4 seeds, respectively. Received November 5, 2008; accepted December 7, 2008; published December 17, 2008.
1 This work was supported by the College of Agricultural and Life Sciences and the Graduate School of the University of Wisconsin (National Institutes of Health grant no. 1R01GM079525 and National Science Foundation grant no. 0209786 [to R.M.A.]). 
2 These authors contributed equally to the article.
3 Present address: Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla, CA 92037. The author responsible for the 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 Mark 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.108.131508 * Corresponding author; e-mail amasino{at}biochem.wisc.edu.
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