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H2A deubiquitinases UBP12/13 are part of the Arabidopsis polycomb group protein system

Nature Plants volume 2, Article number: 16126 (2016) Cite this article

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Abstract

Polycomb group (PcG) proteins form an epigenetic memory system in plants and animals, but interacting proteins are poorly known in plants. Here, we have identified Arabidopsis UBIQUITIN SPECIFIC PROTEASES (USP; UBP in plant and yeasts) 12 and 13 as partners of the plant-specific PcG protein LIKE HETEROCHROMATIN PROTEIN 1 (LHP1). UBP12 binds to chromatin of PcG target genes and is required for histone H3 lysine 27 trimethylation and repression of a subset of PcG target genes. Plants lacking UBP12 and UBP13 developed autonomous endosperm in the absence of fertilization. We have identified UBP12 and UBP13 as new proteins in the plant PcG regulatory network. UBP12 and UBP13 belong to an ancient gene family and represent plant homologues of metazoan USP7. We have found that Drosophila USP7 shares a function in heterochromatic gene repression with UBP12/13 and their homologue UBP26. In summary, we demonstrate that USP7-like proteins are essential for gene silencing in diverse genomic contexts.

PcG proteins function in gene repression and constitute an epigenetic memory system that is conserved in animals and plants. PcG proteins were first described in Drosophila as regulators of Hox genes1. Now, PcG proteins are also known to repress genes during diverse processes in worms, mammals and plants (reviewed in refs 2–4). PcG proteins form large protein complexes such as Polycomb repressive complex (PRC) 1 and PRC2 in animals. Drosophila PRC1 catalyses mono-ubiquitination of lysine 118 in histone H2A (H2AK118ub) by means of its RING subunit. PRC2 catalyses the trimethylation of lysine 27 in histone H3 (H3K27me3). Both PRC1 and PRC2 contribute to gene repression but the underlying mechanisms that prevent transcription are poorly understood. In animals and plants, PRC1 is needed at some genes to recruit PRC2 whereas at other loci PRC1 and PRC2 appear to be recruited independently of each other5–10.

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Figure 1: UBP12 and UBP13 interact with LHP1 in vivo.
Figure 2: UBP12 and UBP13 are required for repression of PcG protein targets.
Figure 3: UBP12 binds to PcG target chromatin and H3K27me3 is locally reduced in ubp13-2 ubp12-1+/– plants.
Figure 4: UBP12 and UBP13 prevent autonomous endosperm development.
Figure 5: UBP12 is an H2Aub deubiquitinase.
Figure 6: Drosophila USP7 is required for heterochromatin formation and transposon repression.

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Acknowledgements

We thank B. Liu (Uppsala) for help with protein expression, E. Savenkov (Uppsala) for providing plasmid pSITE–nYFP-N1-2b, M. Blatt (University of Glasgow) for providing a set of ubiquitin promoter-based vectors with fluorescent tags, X. Cui (Chinese Academy of Science, Beijing) for ubp12-2w ubp13-3 seeds and P. Verrijzer (Erasmus University Medical Centre, Rotterdam) for USP7 mutant flies. We thank TAIR and ABRC for mutant seeds and clones. We thank W. Gruissem for continuous support and providing access to infrastructure. This work was supported by grants from ETH Zurich, the Swedish Research Council and the Knut-and-Alice-Wallenberg Foundation.

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Author notes

  1. Maria Derkacheva and Shujing Liu: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Centre for Plant Biology, SE-75007 Uppsala, Sweden

    Maria Derkacheva, Shujing Liu, Duarte D. Figueiredo, Matthew Gentry, Iva Mozgova, Claudia Köhler & Lars Hennig

  2. Department of Biology and Zurich-Basel Plant Science Centre, ETH Zurich, CH-8092, Zurich, Switzerland

    Maria Derkacheva

  3. Functional Genomics Centre Zurich, University of Zurich/ETH Zürich, CH-8057 Zurich, Switzerland

    Paolo Nanni

  4. Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, SE-10691 Stockholm, Sweden

    Min Tang & Mattias Mannervik

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Contributions

M.D., S.L., D.D.F., M.G., I.M., P.N. and M.T. performed the experiments; M.D., S.L., D.D.F., I.M. and P.N. analysed data; M.D., S.L., M.M., C.K. and L.H. planned the experiments; and M.D., M.M., C.K. and L.H. wrote the manuscript.

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Correspondence to Lars Hennig.

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Derkacheva, M., Liu, S., Figueiredo, D. et al. H2A deubiquitinases UBP12/13 are part of the Arabidopsis polycomb group protein system. Nature Plants 2, 16126 (2016). https://doi.org/10.1038/nplants.2016.126

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