Mutation of a major CG methylase alters genome-wide lncRNA expression in rice

Plant long non-coding RNAs (lncRNAs) function in diverse biological processes, and lncRNA expression is under epigenetic regulation, including by cytosine DNA methylation. However, it remains unclear whether 5-methylcytosine ((5m)C) plays a similar role in different sequence contexts (CG, CHG, and CHH). In this study, we characterized and compared the profiles of genome-wide lncRNA profiles (including long intergenic non-coding RNAs [lincRNAs] and long noncoding natural antisense transcripts [lncNATs]) of a null mutant of the rice DNA methyltransferase 1, OsMET1-2 (designated OsMET1-2(−)(/)(−)) and its isogenic wild type (OsMET1-2(+/+)). The En/Spm transposable element (TE) family, which was heavily methylated in OsMET1-2(+/+), was transcriptionally de-repressed in OsMET1-2(−)(/)(−) due to genome-wide erasure of CG methylation, and this led to abundant production of specific lncRNAs. In addition, RdDM-mediated CHH hypermethylation was increased in the 5′-upstream genomic regions of lncRNAs in OsMET1-2(−)(/)(−). The positive correlation between the expression of lincRNAs and that of their proximal protein-coding genes was also analyzed. Our study shows that CG methylation negatively regulates the TE-related expression of lncRNA and demonstrates that CHH methylation is also involved in the regulation of lncRNA expression.