The octopus genome and the evolution of cephalopod neural and morphological novelties

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Bibliographic Details
Title: The octopus genome and the evolution of cephalopod neural and morphological novelties
Authors: Clifton W. Ragsdale, Judit R. Pungor, Z. Yan Wang, Oleg Simakov, Therese Mitros, Caroline B. Albertin, Eric Edsinger-Gonzales, Daniel S. Rokhsar, Sydney Brenner
Source: Nature
Publisher Information: Springer Science and Business Media LLC, 2015.
Publication Year: 2015
Subject Terms: 0301 basic medicine, DNA Copy Number Variations, Evolution, Ion Channels/genetics, Octopodiformes, Transcription Factors/genetics, DNA Copy Number Variations/genetics, Nervous System, Article, Ion Channels, Evolution, Molecular, 03 medical and health sciences, RNA Editing/genetics, Species Specificity, Animal Structures/anatomy & histology, Animals, Octopodiformes/anatomy & histology, RNA, Messenger, 14. Life underwater, 106001 Allgemeine Biologie, Phylogeny, 0303 health sciences, Genome, Cadherins/genetics, Decapodiformes/genetics, Decapodiformes, Molecular, Animal Structures, Zinc Fingers, Genomics, Cadherins, 3. Good health, 106001 General biology, DNA Transposable Elements/genetics, Organ Specificity, DNA Transposable Elements, Genome/genetics, Nervous System/anatomy & histology, RNA, Messenger/genetics, RNA Editing, Transcription Factors
Description: Coleoid cephalopods (octopus, squid and cuttlefish) are active, resourceful predators with a rich behavioural repertoire. They have the largest nervous systems among the invertebrates and present other striking morphological innovations including camera-like eyes, prehensile arms, a highly derived early embryogenesis and a remarkably sophisticated adaptive colouration system. To investigate the molecular bases of cephalopod brain and body innovations, we sequenced the genome and multiple transcriptomes of the California two-spot octopus, Octopus bimaculoides. We found no evidence for hypothesized whole-genome duplications in the octopus lineage. The core developmental and neuronal gene repertoire of the octopus is broadly similar to that found across invertebrate bilaterians, except for massive expansions in two gene families previously thought to be uniquely enlarged in vertebrates: the protocadherins, which regulate neuronal development, and the C2H2 superfamily of zinc-finger transcription factors. Extensive messenger RNA editing generates transcript and protein diversity in genes involved in neural excitability, as previously described, as well as in genes participating in a broad range of other cellular functions. We identified hundreds of cephalopod-specific genes, many of which showed elevated expression levels in such specialized structures as the skin, the suckers and the nervous system. Finally, we found evidence for large-scale genomic rearrangements that are closely associated with transposable element expansions. Our analysis suggests that substantial expansion of a handful of gene families, along with extensive remodelling of genome linkage and repetitive content, played a critical role in the evolution of cephalopod morphological innovations, including their large and complex nervous systems.
Document Type: Article
Other literature type
Language: English
ISSN: 1476-4687
0028-0836
DOI: 10.1038/nature14668
Access URL: https://www.nature.com/articles/nature14668.pdf
https://pubmed.ncbi.nlm.nih.gov/26268193
https://www.nature.com/articles/nature14668
http://europepmc.org/abstract/MED/26268193
https://www.nature.com/nature/journal/v524/n7564/fig_tab/nature14668_T2.html
https://www.nature.com/articles/nature14668.pdf
https://facultyopinions.com/prime/725718447
https://ui.adsabs.harvard.edu/abs/2015Natur.524..220A/abstract
Rights: CC BY NC SA
Accession Number: edsair.doi.dedup.....7058c19c92b5316f9989dcc7e3618d25
Database: OpenAIRE
Description
Abstract:Coleoid cephalopods (octopus, squid and cuttlefish) are active, resourceful predators with a rich behavioural repertoire. They have the largest nervous systems among the invertebrates and present other striking morphological innovations including camera-like eyes, prehensile arms, a highly derived early embryogenesis and a remarkably sophisticated adaptive colouration system. To investigate the molecular bases of cephalopod brain and body innovations, we sequenced the genome and multiple transcriptomes of the California two-spot octopus, Octopus bimaculoides. We found no evidence for hypothesized whole-genome duplications in the octopus lineage. The core developmental and neuronal gene repertoire of the octopus is broadly similar to that found across invertebrate bilaterians, except for massive expansions in two gene families previously thought to be uniquely enlarged in vertebrates: the protocadherins, which regulate neuronal development, and the C2H2 superfamily of zinc-finger transcription factors. Extensive messenger RNA editing generates transcript and protein diversity in genes involved in neural excitability, as previously described, as well as in genes participating in a broad range of other cellular functions. We identified hundreds of cephalopod-specific genes, many of which showed elevated expression levels in such specialized structures as the skin, the suckers and the nervous system. Finally, we found evidence for large-scale genomic rearrangements that are closely associated with transposable element expansions. Our analysis suggests that substantial expansion of a handful of gene families, along with extensive remodelling of genome linkage and repetitive content, played a critical role in the evolution of cephalopod morphological innovations, including their large and complex nervous systems.
ISSN:14764687
00280836
DOI:10.1038/nature14668