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

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.

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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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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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