Abstract
In eukaryotes, three-dimensional genome organization is critical for transcriptional regulation of gene expression. Long noncoding RNAs (lncRNAs) can modulate chromatin conformation of spatially related genomic locations within the nucleus. Here, we show that the lncRNA APOLO (AUXIN-REGULATED PROMOTER LOOP) recognizes multiple distant independent loci in the Arabidopsis thaliana genome. We found that APOLO targets are not spatially associated in the nucleus and that APOLO recognizes its targets by short sequence complementarity and the formation of DNA-RNA duplexes (R-loops). The invasion of APOLO to the target DNA decoys the plant Polycomb Repressive Complex 1 component LHP1, modulating local chromatin 3D conformation. APOLO lncRNA coordinates the expression of distal unrelated auxin-responsive genes during lateral root development in Arabidopsis. Hence, R-loop formation and chromatin protein decoy mediate trans action of lncRNAs on distant loci.
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•Long noncoding RNAs modulate chromatin three-dimensional conformation in nuclei•Target recognition in trans by long noncoding RNAs can be mediated by R-loop formation•Through R-loop formation, noncoding RNAs can decoy Polycomb proteins from chromatin•R-loops mechanisms may determine regulation of multiple genes by non-coding RNAs
In this work, Ariel et al. demonstrated that the APOLO long noncoding RNA can coordinate expression of multiple genes through sequence complementarity and R-loop formation in plants. Upon target recognition, APOLO can decoy protein complexes and modulate the three-dimensional chromatin conformation to fine-tune gene transcription.