Histone H2B Deubiquitination Is Required for Transcriptional Activation of FLOWERING LOCUS C and for Proper Control of Flowering in Arabidopsis

Robert Jeffrey Schmitz,Mark Robert Doyle,Yosuke Tamada,Richard Mark Amasino,Xiaoyu Zhang

doi:10.1104/pp.108.131508

Robert Jeffrey Schmitz, Mark Robert Doyle + Show 3 more

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https://doi.org/10.1104/pp.108.131508

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Abstract

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.

Highlights

The spectrum of histone modifications at a given locus is a critical determinant for the correct output of gene expression
As the FLOWERING LOCUS C (FLC) locus passes through meiosis and embryogenesis to the generation, it is reset to an active state (Sung and Amasino, 2006; Sheldon et al, 2008)
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)

Summary

Introduction

The spectrum of histone modifications at a given locus is a critical determinant for the correct output of gene expression. MRNA levels of the floral repressor FLOWERING LOCUS C (FLC) and other related family members is decreased. A long exposure to cold, which occurs during winter, enhances the ability to flower in several winter-annual, biennial, or perennial varieties of plants. In winter-annual accessions of Arabidopsis that contain transcriptionally active FLC, histone modifications associated with actively transcribed genes, such as trimethylation of Lys 4 of histone H3 (H3K4me3), diand trimethylation of H3K36 (H3K36me2/me3), and hyperacetylation of H3, are enriched at the FLC locus (He et al, 2004; Kim et al, 2005; Zhao et al, 2005; Sung et al, 2006b; Oh et al, 2008; Pien et al, 2008; Xu et al, 2008). As the FLC locus passes through meiosis and embryogenesis to the generation, it is reset to an active state (Sung and Amasino, 2006; Sheldon et al, 2008)

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