SHOOT GROWTH1 Maintains Arabidopsis Epigenomes by Regulating <i>IBM1</i>

Maintaining correct DNA and histone methylation patterns is essential for the development of all eukaryotes. In Arabidopsis, we identified SHOOT GROWTH1 (SG1), a novel protein involved in the control of gene methylation. SG1 contains both a Bromo-Adjacent Homology (BAH) domain found in several chromatin regulators and an RNA-Recognition Motif (RRM). The sg1 mutations are associated with drastic pleiotropic phenotypes. The mutants degenerate after few generations and are similar to mutants of the histone demethylase INCREASE IN BONSAI METHYLATION1 (IBM1). A methylome analysis of sg1 mutants revealed a large number of gene bodies hypermethylated in the cytosine CHG context, associated with an increase in di-methylation of lysine 9 on histone H3 tail (H3K9me2), an epigenetic mark normally found in silenced transposons. The sg1 phenotype is suppressed by mutations in genes encoding the DNA methyltransferase CHROMOMETHYLASE3 (CMT3) or the histone methyltransferase KRYPTONITE (KYP), indicating that SG1 functions antagonistically to CMT3 or KYP. We further show that the IBM1 transcript is not correctly processed in sg1, and that the functional IBM1 transcript complements sg1. Altogether, our results suggest a function for SG1 in the maintenance of genome integrity by regulating IBM1.维持正确的DNA与组蛋白甲基化模式，对所有真核生物的发育至关重要。在拟南芥（Arabidopsis）中，我们鉴定到SHOOT GROWTH1（SG1）——一种参与调控基因甲基化的新型蛋白质。SG1同时包含在多种染色质调控因子中存在的溴相邻同源（Bromo-Adjacent Homology，BAH）结构域，以及RNA识别基序（RNA-Recognition Motif，RRM）。sg1突变体表现出显著的多效性表型，且在传代数代后发生退化，其表型与组蛋白去甲基化酶INCREASE IN BONSAI METHYLATION1（IBM1）的突变体相似。对sg1突变体的甲基化组分析显示，大量基因体在胞嘧啶CHG位点发生超甲基化，这与组蛋白H3尾部第9位赖氨酸的二甲基化（H3K9me2）水平升高相关；H3K9me2是一类通常存在于沉默转座子中的表观遗传标记。编码DNA甲基转移酶CHROMOMETHYLASE3（CMT3）或组蛋白甲基转移酶KRYPTONITE（KYP）的基因突变后，可抑制sg1的表型，这表明SG1的功能与CMT3或KYP相互拮抗。我们进一步证实，IBM1的转录本在sg1突变体中无法被正确加工，且功能性IBM1转录本可互补恢复sg1突变体的表型。综上，本研究结果表明，SG1通过调控IBM1参与维持基因组完整性。