The gold-ringed octopus (Amphioctopus fangsiao) genome and cerebral single-nucleus transcriptomes provide insights into the evolution of karyotype and neural novelties.
Cephalopod
Chromosome
Genome
Octopoda
Single cell
Supra-esophageal brain
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
27 12 2022
27 12 2022
Historique:
received:
14
06
2022
accepted:
08
12
2022
entrez:
27
12
2022
pubmed:
28
12
2022
medline:
30
12
2022
Statut:
epublish
Résumé
Coleoid cephalopods have distinctive neural and morphological characteristics compared to other invertebrates. Early studies reported massive genomic rearrangements occurred before the split of octopus and squid lineages (Proc Natl Acad Sci U S A 116:3030-5, 2019), which might be related to the neural innovations of their brain, yet the details remain elusive. Here we combine genomic and single-nucleus transcriptome analyses to investigate the octopod chromosome evolution and cerebral characteristics. We present a chromosome-level genome assembly of a gold-ringed octopus, Amphioctopus fangsiao, and a single-nucleus transcriptome of its supra-esophageal brain. Chromosome-level synteny analyses estimate that the chromosomes of the ancestral octopods experienced multiple chromosome fission/fusion and loss/gain events by comparing with the nautilus genome as outgroup, and that a conserved genome organization was detected during the evolutionary process from the last common octopod ancestor to their descendants. Besides, protocadherin, GPCR, and C2H2 ZNF genes are thought to be highly related to the neural innovations in cephalopods (Nature 524:220-4, 2015), and the chromosome analyses pinpointed several collinear modes of these genes on the octopod chromosomes, such as the collinearity between PCDH and C2H2 ZNF, as well as between GPCR and C2H2 ZNF. Phylogenetic analyses show that the expansion of the octopod protocadherin genes is driven by a tandem-duplication mechanism on one single chromosome, including two separate expansions at 65 million years ago (Ma) and 8-14 Ma, respectively. Furthermore, we identify eight cell types (i.e., cholinergic and glutamatergic neurons) in the supra-esophageal brain of A. fangsiao, and the single-cell expression analyses reveal the co-expression of protocadherin and GPCR in specific neural cells, which may contribute to the neural development and signal transductions in the octopod brain. The octopod genome analyses reveal the dynamic evolutionary history of octopod chromosomes and neural-related gene families. The single-nucleus transcriptomes of the supra-esophageal brain indicate their cellular heterogeneities and functional interactions with other tissues (i.e., gill), which provides a foundation for further octopod cerebral studies.
Sections du résumé
BACKGROUND
Coleoid cephalopods have distinctive neural and morphological characteristics compared to other invertebrates. Early studies reported massive genomic rearrangements occurred before the split of octopus and squid lineages (Proc Natl Acad Sci U S A 116:3030-5, 2019), which might be related to the neural innovations of their brain, yet the details remain elusive. Here we combine genomic and single-nucleus transcriptome analyses to investigate the octopod chromosome evolution and cerebral characteristics.
RESULTS
We present a chromosome-level genome assembly of a gold-ringed octopus, Amphioctopus fangsiao, and a single-nucleus transcriptome of its supra-esophageal brain. Chromosome-level synteny analyses estimate that the chromosomes of the ancestral octopods experienced multiple chromosome fission/fusion and loss/gain events by comparing with the nautilus genome as outgroup, and that a conserved genome organization was detected during the evolutionary process from the last common octopod ancestor to their descendants. Besides, protocadherin, GPCR, and C2H2 ZNF genes are thought to be highly related to the neural innovations in cephalopods (Nature 524:220-4, 2015), and the chromosome analyses pinpointed several collinear modes of these genes on the octopod chromosomes, such as the collinearity between PCDH and C2H2 ZNF, as well as between GPCR and C2H2 ZNF. Phylogenetic analyses show that the expansion of the octopod protocadherin genes is driven by a tandem-duplication mechanism on one single chromosome, including two separate expansions at 65 million years ago (Ma) and 8-14 Ma, respectively. Furthermore, we identify eight cell types (i.e., cholinergic and glutamatergic neurons) in the supra-esophageal brain of A. fangsiao, and the single-cell expression analyses reveal the co-expression of protocadherin and GPCR in specific neural cells, which may contribute to the neural development and signal transductions in the octopod brain.
CONCLUSIONS
The octopod genome analyses reveal the dynamic evolutionary history of octopod chromosomes and neural-related gene families. The single-nucleus transcriptomes of the supra-esophageal brain indicate their cellular heterogeneities and functional interactions with other tissues (i.e., gill), which provides a foundation for further octopod cerebral studies.
Identifiants
pubmed: 36575497
doi: 10.1186/s12915-022-01500-2
pii: 10.1186/s12915-022-01500-2
pmc: PMC9795677
doi:
Substances chimiques
Protocadherins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
289Subventions
Organisme : National Natural Science Foundation of China
ID : 31672257
Organisme : National Natural Science Foundation of China
ID : 32170536
Organisme : Fundamental Research Funds for Central Universities of the Central South University
ID : 201822022
Informations de copyright
© 2022. The Author(s).
Références
Nat Protoc. 2016 Sep;11(9):1650-67
pubmed: 27560171
Nucleic Acids Res. 1997 Mar 1;25(5):955-64
pubmed: 9023104
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Cell Syst. 2016 May 25;2(5):347-54
pubmed: 27185547
Nature. 2015 Aug 13;524(7564):220-4
pubmed: 26268193
Elife. 2023 Jan 03;12:
pubmed: 36594460
Front Physiol. 2018 Jul 20;9:952
pubmed: 30079030
Innovation (Camb). 2021 Jul 01;2(3):100141
pubmed: 34557778
Gigascience. 2020 May 1;9(5):
pubmed: 32352532
Nucleic Acids Res. 2012 Apr;40(7):e49
pubmed: 22217600
BMC Bioinformatics. 2003 Sep 11;4:41
pubmed: 12969510
Genome Biol. 2009;10(3):R25
pubmed: 19261174
Nat Ecol Evol. 2018 Jan;2(1):141-151
pubmed: 29203924
Sci Data. 2019 Apr 1;6(1):13
pubmed: 30931949
Gigascience. 2018 Nov 1;7(11):
pubmed: 30256935
Cell. 2014 Dec 18;159(7):1665-80
pubmed: 25497547
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Science. 2017 Apr 7;356(6333):92-95
pubmed: 28336562
Nucleic Acids Res. 2016 May 19;44(9):e89
pubmed: 26893356
Nature. 2012 Oct 4;490(7418):49-54
pubmed: 22992520
Cell Syst. 2016 Jul;3(1):95-8
pubmed: 27467249
Mol Biol Evol. 2019 Jul 1;36(7):1507-1520
pubmed: 30980073
Curr Biol. 2022 Jan 10;32(1):97-110.e4
pubmed: 34798049
Bioinformatics. 2009 Sep 1;25(17):2286-8
pubmed: 19535536
Proc Natl Acad Sci U S A. 2019 Feb 19;116(8):3030-3035
pubmed: 30635418
Biol Bull. 2006 Jun;210(3):308-17
pubmed: 16801504
Nat Commun. 2022 Apr 21;13(1):2172
pubmed: 35449136
Curr Biol. 2016 Oct 24;26(20):R965-R971
pubmed: 27780070
Genome Res. 2004 May;14(5):988-95
pubmed: 15123596
Genome Res. 2009 Jan;19(1):143-9
pubmed: 18838612
Cell Rep. 2017 Oct 24;21(4):1077-1088
pubmed: 29069589
Mol Ecol Resour. 2020 Nov;20(6):1572-1582
pubmed: 32603549
Gigascience. 2018 Apr 1;7(4):
pubmed: 29617765
Semin Cell Dev Biol. 2017 Sep;69:151-157
pubmed: 28627384
Gigascience. 2021 Apr 23;10(4):
pubmed: 33891010
Comp Cytogenet. 2017 Jul 25;11(3):477-494
pubmed: 29093799
Nat Ecol Evol. 2021 Jul;5(7):927-938
pubmed: 33972735
Nat Genet. 2000 May;25(1):25-9
pubmed: 10802651
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
Genome Res. 2017 May;27(5):737-746
pubmed: 28100585
Mol Ecol Resour. 2020 Jan;20(1):348-355
pubmed: 31599058
Nucleic Acids Res. 1999 Jan 15;27(2):573-80
pubmed: 9862982
Genome Biol Evol. 2021 Jan 7;13(1):
pubmed: 33320175
Bioinformatics. 2003 Oct;19 Suppl 2:ii215-25
pubmed: 14534192
Nat Ecol Evol. 2017 Apr 03;1(5):120
pubmed: 28812685
Sci Data. 2019 Feb 19;6:190022
pubmed: 30778257
Mol Ecol Resour. 2017 Jul;17(4):686-693
pubmed: 27768249
Genome Biol Evol. 2020 Jun 1;12(6):905-910
pubmed: 32467969
Nat Commun. 2017 May 16;8:15451
pubmed: 28508897
Nucleic Acids Res. 2019 Jul 2;47(W1):W256-W259
pubmed: 30931475
Genome Res. 2009 Sep;19(9):1639-45
pubmed: 19541911
Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3547-52
pubmed: 8622973
Genome Res. 2017 May;27(5):722-736
pubmed: 28298431
Nucleic Acids Res. 2000 Jan 1;28(1):45-8
pubmed: 10592178
Nat Commun. 2022 May 4;13(1):2427
pubmed: 35508532
Zoolog Sci. 2002 Jul;19(7):763-71
pubmed: 12149577
BMC Genomics. 2006 Dec 28;7:327
pubmed: 17194304
Curr Biol. 2020 Nov 2;30(21):4322-4327.e3
pubmed: 32916119
Genome Biol. 2019 Nov 14;20(1):238
pubmed: 31727128
Mol Biol Evol. 2020 May 1;37(5):1530-1534
pubmed: 32011700
C R Biol. 2004 Feb;327(2):133-8
pubmed: 15060984
Biochem Biophys Res Commun. 2012 Mar 23;419(4):779-81
pubmed: 22390928
Gene. 2011 Sep 1;483(1-2):63-71
pubmed: 21672613
Curr Protoc Bioinformatics. 2018 Dec;64(1):e56
pubmed: 30332532
Nat Methods. 2020 Feb;17(2):155-158
pubmed: 31819265
Nature. 2013 Jan 24;493(7433):526-31
pubmed: 23254933
Exp Neurobiol. 2018 Aug;27(4):257-266
pubmed: 30181688
BMC Bioinformatics. 2004 Aug 19;5:113
pubmed: 15318951
Nat Methods. 2015 Jan;12(1):59-60
pubmed: 25402007
Bioinformatics. 2009 Aug 1;25(15):1972-3
pubmed: 19505945
J Mol Biol. 1997 Apr 25;268(1):78-94
pubmed: 9149143
Front Biosci (Schol Ed). 2010 Jan 01;2(2):764-71
pubmed: 20036982
Mol Ecol Resour. 2022 Jan;22(1):15-27
pubmed: 34085392
Genome Biol Evol. 2011;3:1150-63
pubmed: 21859805
PLoS One. 2014 Nov 19;9(11):e112963
pubmed: 25409509
Proc Biol Sci. 2019 Feb 27;286(1897):20182929
pubmed: 30963849
Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14893-8
pubmed: 20679223
Nat Commun. 2022 Nov 30;13(1):7392
pubmed: 36450803
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W265-8
pubmed: 17485477
Genome Biol. 2008 Jan 11;9(1):R7
pubmed: 18190707
Nat Commun. 2020 Apr 8;11(1):1657
pubmed: 32269225
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
Nature. 2003 Aug 28;424(6952):1061-5
pubmed: 12944969
Genome Biol. 2015 Dec 01;16:259
pubmed: 26619908
BMC Biol. 2022 Dec 27;20(1):289
pubmed: 36575497
Nat Ecol Evol. 2019 Jan;3(1):96-104
pubmed: 30510179
Bioinformatics. 2004 Nov 1;20(16):2878-9
pubmed: 15145805
Front Genet. 2019 Nov 20;10:1158
pubmed: 31824566
Gigascience. 2020 Jan 1;9(1):
pubmed: 31942620
Gigascience. 2020 Nov 10;9(11):
pubmed: 33175168
DNA Res. 2018 Dec 1;25(6):655-665
pubmed: 30295708
Gigascience. 2019 Jul 1;8(7):
pubmed: 31289832
BMC Bioinformatics. 2004 May 14;5:59
pubmed: 15144565