Research ArticlePlant biology

The histone deubiquitinase OTLD1 targets euchromatin to regulate plant growth

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Sci. Signal.  20 Dec 2016:
Vol. 9, Issue 459, pp. ra125
DOI: 10.1126/scisignal.aaf6767

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Targeting euchromatin to promote plant growth

Posttranslational modifications of histones, such as ubiquitination, acetylation, and methylation, influence gene expression. Heterochromatin, the tightly packed form of chromatin associated with gene silencing, and euchromatin, the loosely packed chromatin of actively transcribed genes, are characterized by distinct types of histone modifications. Of the 50 deubiquitinases encoded by the Arabidopsis thaliana genome, only 2 are known to target histones, UBP26 and OTLD1. Keren and Citovsky found that OTLD1 promoted overall plant growth, likely by stimulating cell growth rather than proliferation. From a panel of genes that control plant growth, five were repressed by overexpression of OTLD1. OTLD1 associated with chromatin at the promoters of each of these genes and promoted epigenetic remodeling of the euchromatin-associated histone modifications, including loss of ubiquitination, acetylation, and methylation. Thus, OTLD1 promotes plant growth by stimulating the removal of euchromatic histone marks, thereby repressing the expression of genes that fine-tune growth.

Abstract

Histone monoubiquitination is associated with active chromatin and plays an important role in epigenetic regulation of gene expression in plants. Deubiquitinating enzymes remove the ubiquitin group from histones and thereby contribute to gene repression. The Arabidopsis thaliana genome encodes 50 deubiquitinases, yet only 2 of them—UBP26 and OTLD1, members of the USP/UBP (ubiquitin-specific protease and ubiquitin-binding protein) and OTU (ovarian tumor protease) deubiquitinase families—are known to target histones. Furthermore, UBP26 is the only plant histone deubiquitinase for which the functional role has been characterized in detail. We used gain- and loss-of-function alleles of OTLD1 to examine its role in the plant life cycle and showed that OTLD1 stimulates plant growth, increases cell size, and induces transcriptional repression of five major regulators of plant organ growth and development: GA20OX, WUS, OSR2, ARL, and ABI5. OTLD1 associated with chromatin at each of these target genes and promoted the removal of euchromatic histone acetylation, ubiquitination, and methylation marks. Thus, these data indicate that OTLD1 promotes the concerted epigenetic regulation of a set of genes that collectively limit plant growth.

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