pealeii, the first cephalopod to be edited 22. The value of these models has recently taken a leap forward with the development of CRISPR-mediated gene manipulation in D. More recently, these squid are models of cephalopod behavior 16, 17, 18, development 19, and cephalopod-derived biomaterials 20, 21. Famously, the mechanisms underlying the propagation of action potentials were deciphered using experimental preparations of loliginid giant axons, which transmit signals from the stellate ganglion to the muscular mantle 14, 15. Loliginid squid of the genera Loligo and Doryteuthis have played critical roles in the development of molecular and cellular neuroscience 13. To address these questions, we sequenced the genome of a single Atlantic longfin inshore squid Doryteuthis (formerly Loligo) pealeii, also known as the Boston market squid, and developed complementary transcript resources for analyzing RNA editing (Fig. The relative contribution of these and other factors to complexity and novelty in cephalopods has remained mysterious, in part due to the lack of complete chromosome-scale genome sequences and an absence of sampling of RNAs across tissues. Despite differences in genome duplication and RNA editing, notable convergent gene family expansions have occurred in vertebrates and cephalopods, but using distinct mechanisms 5. In vertebrates, editing is largely limited to transcribed transposable elements only a handful of important nervous system proteins are functionally altered by edits 11, 12. At the transcriptional level, messenger RNA editing has been proposed as a potent mechanism for expanding protein diversity in coleoid cephalopods 5, 7, 8, 9, 10. Nevertheless, coleoid cephalopod chromosome numbers are dramatically larger than those of other molluscs 6, suggesting a possible role for chromosome-disrupting processes in coleoid evolution. At a genomic level, vertebrate complexity has been hypothesized to be linked to repeated rounds of whole genome duplication 3, 4, but this mechanism is not in play in cephalopods 5. The complex behavioral repertoire of coleoid cephalopods (squid, cuttlefish, and octopus) is orchestrated by the largest of invertebrate nervous systems, which arose by an independent, radically different, and largely unknown evolutionary trajectory compared with that of vertebrates 1, 2. We conclude that coleoid novelty is mediated in part by substantial genome reorganization, gene family expansion, and tissue-dependent mRNA editing. We find that a known coleoid hallmark, extensive A-to-I mRNA editing, displays two fundamentally distinct patterns: one exclusive to the nervous system and concentrated in genic sequences, the other widespread and directed toward repetitive elements. The coleoid genomes feature multi-megabase, tandem arrays of genes associated with brain development and cephalopod-specific innovations. The genomes of the soft-bodied (coleoid) cephalopods are highly rearranged relative to other extant molluscs, indicating an intense, early burst of genome restructuring.
To investigate the genomic underpinnings of these features, we assembled the chromosomes of the Boston market squid, Doryteuthis (Loligo) pealeii, and the California two-spot octopus, Octopus bimaculoides, and compared them with those of the Hawaiian bobtail squid, Euprymna scolopes. Cephalopods are known for their large nervous systems, complex behaviors and morphological innovations.
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