Long noncoding RNAs (lncRNAs) are key regulators of chromatin state, yet the 
nature and sites of RNA-chromatin interaction are mostly unknown. Here we 
introduce Chromatin Isolation by RNA Purification (ChIRP), where tiling 
oligonucleotides retrieve specific lncRNAs with bound protein and DNA sequences, 
which are enumerated by deep sequencing. ChIRP-seq of three lncRNAs reveal that 
RNA occupancy sites in the genome are focal, sequence-specific, and numerous. 
Drosophila roX2 RNA occupies male X-linked gene bodies with increasing tendency 
toward the 3' end, peaking at CES sites. Human telomerase RNA TERC occupies 
telomeres and Wnt pathway genes. HOTAIR lncRNA preferentially occupies a GA-rich 
DNA motif to nucleate broad domains of Polycomb occupancy and histone H3 lysine 
27 trimethylation. HOTAIR occupancy occurs independently of EZH2, suggesting the 
order of RNA guidance of Polycomb occupancy. ChIRP-seq is generally applicable 
to illuminate the intersection of RNA and chromatin with newfound precision 
genome wide.