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Abstract
We introduce APEX-seq, a method for RNA sequencing based on direct proximity labeling
of RNA using the peroxidase enzyme APEX2. APEX-seq in nine distinct subcellular locales
produced a nanometer-resolution spatial map of the human transcriptome as a resource,
revealing extensive patterns of localization for diverse RNA classes and transcript
isoforms. We uncover a radial organization of the nuclear transcriptome, which is
gated at the inner surface of the nuclear pore for cytoplasmic export of processed
transcripts. We identify two distinct pathways of messenger RNA localization to mitochondria,
each associated with specific sets of transcripts for building complementary macromolecular
machines within the organelle. APEX-seq should be widely applicable to many systems,
enabling comprehensive investigations of the spatial transcriptome. A newly-developed
technique reveals the subcellular transcriptomes at many landmarks in the nucleus
and cytosol, and connects mRNA localization to genome architecture, protein location
and local-translation mechanisms.