Histone demethylase IBM1-mediated meiocyte gene expression ensures meiotic chromosome synapsis and recombination

Author summaryMeiosis is essential for sexual reproduction in most eukaryotes, including plants. In recent years, epigenetic modification such as DNA methylation, histone modifications and histone variants has been shown to play essential roles in meiosis likely by regulating chromatin structure and gene expression. However, the role of histone demethylases in regulating meiotic progression remains largely uncharacterized. Here we show that INCREASE IN BONSAI METHYLATION 1 (IBM1) is required for normal meiotic progression in Arabidopsis. Its mutation causes multiple meiotic defects of synapsis and recombination, and reduced fertility. Genetic analyses demonstrate that these ibm1 defects are restored by mutations in either SUVH4/KYP (SUPPRESSOR OF VARIEGATION HOMOLOG 4/ KRYPTONITE) or CMT3 which are associated with DNA CHG methylation. We further show that IBM1 affects expression levels of a large number of genes specifically in meiocytes. Most of them are rescued in ibm1 cmt3 double mutant and are highly correlated with a significant reduction of gene body CHG methylation, including known meiotic Arabidopsis-mei2-like genes AML3-5. Consistently, the aml3/4/5 triple mutants shows similar meiotic defects to ibm1 single mutant. Together, our results provide demonstration of IBM1 in meiosis, increasing the spectrum of substrate specificity of key epigenetic regulator histone demethylase. Histone methylation and demethylation play important roles in plant growth and development, but the involvement of histone demethylation during meiosis is poorly understood. Here we show that disruption of Arabidopsis thaliana INCREASE IN BONSAI METHYLATION 1 (IBM1) causes incomplete synapsis, chromosome entanglement and reduction of recombination during meiosis, leading to sterility. Interestingly, these ibm1 meiotic defects are rescued by mutations in either SUVH4/KYP or CMT3. Using transcriptomic analyses we show that mutation of IBM1 down-regulates thousands of genes expressed in meiocytes, and that expression of about 38% of these genes are restored to wild type levels in ibm1 cmt3 double mutants. Changes in the expression of 437 of these, including the ARABIDOPSIS MEI2-LIKE AML3-5 genes, are correlated with a significant reduction of gene body CHG methylation. Consistently, the aml3 aml4 aml5 triple have defects in synapsis and chromosome entanglement similar to ibm1. Genetic analysis shows that aml3 aml4 aml5 ibm1 quadruple mutants resembles the ibm1 single mutant. Strikingly, over expression of AML5 in ibm1 can partially rescue the ibm1 meiotic defects. Taken together, our results demonstrate that histone demethylase IBM1 is required for meiosis likely via coordinated regulation of meiocyte gene expression during meiosis.