The majority of transcripts in the squid nervous system are extensively recoded by A-to-I RNA editing

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Abstract

RNA editing by adenosine deamination alters genetic information from the genomic blueprint. When it recodes mRNAs, it gives organisms the option to express diverse, functionally distinct, protein isoforms. All eumetazoans, from cnidarians to humans, express RNA editing enzymes. However, transcriptome-wide screens have only uncovered about 25 transcripts harboring conserved recoding RNA editing sites in mammals and several hundred recoding sites in Drosophila. These studies on few established models have led to the general assumption that recoding by RNA editing is extremely rare. Here we employ a novel bioinformatic approach with extensive validation to show that the squid Doryteuthis pealeii recodes proteins by RNA editing to an unprecedented extent. We identify 57,108 recoding sites in the nervous system, affecting the majority of the proteins studied. Recoding is tissue-dependent, and enriched in genes with neuronal and cytoskeletal functions, suggesting it plays an important role in brain physiology.

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Shahar Alon

George S Wise Faculty of Life Sciences, Department of Neurobiology, Tel Aviv University, Tel Aviv, Israel

Competing interests
The authors declare that no competing interests exist.
Sandra C Garrett

Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center, Farmington, United States

Competing interests
The authors declare that no competing interests exist.
Erez Y Levanon

Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel

Competing interests
The authors declare that no competing interests exist.
Sara Olson

Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center, Farmington, United States

Competing interests
The authors declare that no competing interests exist.
Brenton R Graveley

Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center, Farmington, United States

Competing interests
The authors declare that no competing interests exist.
Joshua J C Rosenthal

Institute of Neurobiology, University of Puerto Rico Medical Sciences Campus, San Juan, Puerto Rico

Competing interests
The authors declare that no competing interests exist.
Eli Eisenberg

Sagol school of Neuroscience, Tel Aviv University, Tel Aviv, Israel

For correspondence
elieis@post.tau.ac.il

Competing interests
The authors declare that no competing interests exist.

Ethics

Animal experimentation: Animal experimentation was conducted in accordance to the guidelines of the Marine Biological Laboratory in Woods Hole, Massachusetts.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.