The Arabidopsis GyraseB3 contributes to transposon silencing by promoting histone deacetylation

Abstract

DNA methylation and histone modifications are key epigenetic marks controlling chromatin structure, gene expression and transposable element (TE) activity. In plants, the histone demethylase INCREASE IN BONSAI METHYLATION1 (IBM1) prevents heterochromatic silencing marks from accumulating on actively transcribed genes. Through a genetic screen of mutants defective in IBM1 production, we identified suppressor mutations in genes essential for maintaining balanced genome-wide epigenetic states. The gyrb3 mutation partly reversed DNA hypermethylation in IBM1-deficient plants, revealing a novel role for GyrB3, a nuclear protein combining domains from cyanobacterial gyrases and ELM2/SANT proteins involved in histone acetylation. In gyrb3 mutants, TEs exhibit transcriptional activity, showing reduced DNA methylation and increased histone H3 acetylation, both of which are epigenetic marks associated with expression activation. GyrB3 physically interacts with histone deacetylases like HISTONE DEACETYLASE6 (HDA6), likely mediating their activities at TEs. The functional overlap between HDA6 and GyrB3 is further supported by the observation that, similar to gyrb3, a mutation in hda6 suppresses the Ibm2 phenotype. Our findings reinforce that histone deacetylation is essential for TE silencing and that loss of IBM1 in plants abolished the frontiers between genes and TEs, emphasizing its importance in maintaining epigenomic stability. Key PointsO_LIIBM1 is a histone demethylase that safeguards actively transcribed genes from inappropriate heterochromatic silencing, thereby preserving their function and epigenomic integrity. A gyrb3 mutant suppresses the developmental abnormalities observed in ibm1 or ibm2 mutants. C_LIO_LIGyrB3, though misannotated as a plant gyrase, appears to have evolved away from its conventional role and instead functions in epigenetic regulation. C_LIO_LIGyrB3 is a nuclear protein that interacts with histone deacetylases such as HDA6 to repress transposon activity; mutating GYRB3 results in elevated transposon expression, driven by reduced DNA methylation and increased histone acetylation. C_LI