Emergence of novel cephalopod gene regulation and expression through large-scale genome reorganization.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
21 04 2022
21 04 2022
Historique:
received:
19
08
2020
accepted:
28
03
2022
entrez:
22
4
2022
pubmed:
23
4
2022
medline:
26
4
2022
Statut:
epublish
Résumé
Coleoid cephalopods (squid, cuttlefish, octopus) have the largest nervous system among invertebrates that together with many lineage-specific morphological traits enables complex behaviors. The genomic basis underlying these innovations remains unknown. Using comparative and functional genomics in the model squid Euprymna scolopes, we reveal the unique genomic, topological, and regulatory organization of cephalopod genomes. We show that coleoid cephalopod genomes have been extensively restructured compared to other animals, leading to the emergence of hundreds of tightly linked and evolutionary unique gene clusters (microsyntenies). Such novel microsyntenies correspond to topological compartments with a distinct regulatory structure and contribute to complex expression patterns. In particular, we identify a set of microsyntenies associated with cephalopod innovations (MACIs) broadly enriched in cephalopod nervous system expression. We posit that the emergence of MACIs was instrumental to cephalopod nervous system evolution and propose that microsyntenic profiling will be central to understanding cephalopod innovations.
Identifiants
pubmed: 35449136
doi: 10.1038/s41467-022-29694-7
pii: 10.1038/s41467-022-29694-7
pmc: PMC9023564
doi:
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2172Subventions
Organisme : Austrian Science Fund FWF
ID : P 30686
Pays : Austria
Organisme : Wellcome Trust
ID : FC001003
Pays : United Kingdom
Organisme : Medical Research Council
ID : FC001003
Pays : United Kingdom
Organisme : Cancer Research UK
ID : FC0001003
Pays : United Kingdom
Informations de copyright
© 2022. The Author(s).
Références
Ritschard, E. A. et al. Coupled genomic evolutionary histories as signatures of organismal innovations in cephalopods: co-evolutionary signatures across levels of genome organization may shed light on functional linkage and origin of cephalopod novelties. BioEssays N. Rev. Mol. Cell. Dev. Biol. 41, e1900073 (2019).
Albertin, C. B. et al. The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524, 220–224 (2015).
doi: 10.1038/nature14668
pubmed: 26268193
pmcid: 4795812
Belcaid, M. et al. Symbiotic organs shaped by distinct modes of genome evolution in cephalopods. Proc. Natl Acad. Sci. USA 116, 3030–3035 (2019).
doi: 10.1073/pnas.1817322116
pubmed: 30635418
pmcid: 6386654
Engström, P. G., Ho Sui, S. J., Drivenes, O., Becker, T. S. & Lenhard, B. Genomic regulatory blocks underlie extensive microsynteny conservation in insects. Genome Res. 17, 1898–1908 (2007).
doi: 10.1101/gr.6669607
pubmed: 17989259
pmcid: 2099597
Irimia, M. et al. Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints. Genome Res. 22, 2356–2367 (2012).
doi: 10.1101/gr.139725.112
pubmed: 22722344
pmcid: 3514665
Simakov, O. et al. Insights into bilaterian evolution from three spiralian genomes. Nature 493, 526–531 (2013).
doi: 10.1038/nature11696
pubmed: 23254933
Kikuta, H. et al. Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates. Genome Res. 17, 545–555 (2007).
doi: 10.1101/gr.6086307
pubmed: 17387144
pmcid: 1855176
Zimmermann, B., Robert, N. S. M., Technau, U. & Simakov, O. Ancient animal genome architecture reflects cell type identities. Nat. Ecol. Evol. 3, 1289–1293 (2019).
doi: 10.1038/s41559-019-0946-7
pubmed: 31383947
McFall-Ngai, M. J. & Ruby, E. G. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 254, 1491–1494 (1991).
doi: 10.1126/science.1962208
pubmed: 1962208
Nyholm, S. V. & McFall-Ngai, M. J. A lasting symbiosis: how the Hawaiian bobtail squid finds and keeps its bioluminescent bacterial partner. Nat. Rev. Microbiol. https://doi.org/10.1038/s41579-021-00567-y (2021).
Wang, S. et al. Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat. Ecol. Evol. 1, s41559-017–0120–017 (2017).
doi: 10.1038/s41559-017-0120
Zhang, Y. et al. The genome of Nautilus pompilius illuminates eye evolution and biomineralization. Nat. Ecol. Evol. 5, 927–938 (2021).
doi: 10.1038/s41559-021-01448-6
pubmed: 33972735
pmcid: 8257504
van Berkum, N. L. et al. Hi-C: a method to study the three-dimensional architecture of genomes. J. Vis. Exp. JoVE https://doi.org/10.3791/1869 (2010).
Friedman, N. & Rando, O. J. Epigenomics and the structure of the living genome. Genome Res. 25, 1482–1490 (2015).
doi: 10.1101/gr.190165.115
pubmed: 26430158
pmcid: 4579333
Dali, R. & Blanchette, M. A critical assessment of topologically associating domain prediction tools. Nucleic Acids Res. 45, 2994–3005 (2017).
doi: 10.1093/nar/gkx145
pubmed: 28334773
pmcid: 5389712
Cubeñas-Potts, C. & Corces, V. G. Architectural proteins, transcription, and the three-dimensional organization of the genome. FEBS Lett. 589, 2923–2930 (2015).
doi: 10.1016/j.febslet.2015.05.025
pubmed: 26008126
pmcid: 4598269
Symmons, O. et al. Functional and topological characteristics of mammalian regulatory domains. Genome Res. 24, 390–400 (2014).
doi: 10.1101/gr.163519.113
pubmed: 24398455
pmcid: 3941104
Heger, P., Marin, B., Bartkuhn, M., Schierenberg, E. & Wiehe, T. The chromatin insulator CTCF and the emergence of metazoan diversity. Proc. Natl Acad. Sci. USA 109, 17507–17512 (2012).
doi: 10.1073/pnas.1111941109
pubmed: 23045651
pmcid: 3491479
Rubio, E. D. et al. CTCF physically links cohesin to chromatin. Proc. Natl Acad. Sci. USA 105, 8309–8314 (2008).
doi: 10.1073/pnas.0801273105
pubmed: 18550811
pmcid: 2448833
Filippova, G. N. et al. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol. Cell. Biol. 16, 2802–2813 (1996).
doi: 10.1128/MCB.16.6.2802
pubmed: 8649389
pmcid: 231272
Acemel, R. D., Maeso, I. & Gómez-Skarmeta, J. L. Topologically associated domains: a successful scaffold for the evolution of gene regulation in animals. Wiley Interdiscip. Rev. Dev. Biol. 6, e265 (2017).
Lazar, N. H. et al. Epigenetic maintenance of topological domains in the highly rearranged gibbon genome. Genome Res. 28, 983–997 (2018).
doi: 10.1101/gr.233874.117
pubmed: 29914971
pmcid: 6028127
Touceda-Suárez, M. et al. Ancient genomic regulatory blocks are a source for regulatory gene deserts in vertebrates after whole-genome duplications. Mol. Biol. Evol. 37, 2857–2864 (2020).
doi: 10.1093/molbev/msaa123
pubmed: 32421818
pmcid: 7530604
Kryuchkova-Mostacci, N. & Robinson-Rechavi, M. Tissue-specificity of gene expression diverges slowly between orthologs, and rapidly between paralogs. PLOS Comput. Biol. 12, e1005274 (2016).
doi: 10.1371/journal.pcbi.1005274
pubmed: 28030541
pmcid: 5193323
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213 (2013).
doi: 10.1038/nmeth.2688
pubmed: 24097267
pmcid: 3959825
Hood, K. N. et al. Endoplasmic reticulum stress contributes to the loss of newborn hippocampal neurons after traumatic brain injury. J. Neurosci. 38, 2372–2384 (2018).
doi: 10.1523/JNEUROSCI.1756-17.2018
pubmed: 29386258
pmcid: 5830522
Wang, Y. et al. The role of E2F1-topoIIβ signaling in regulation of cell cycle exit and neuronal differentiation of human SH-SY5Y cells. Differ. Res. Biol. Divers 104, 1–12 (2018).
Lu, C. et al. Overexpression of NEUROG2 and NEUROG1 in human embryonic stem cells produces a network of excitatory and inhibitory neurons. FASEB J. 33, 5287–5299 (2019).
doi: 10.1096/fj.201801110RR
pubmed: 30698461
pmcid: 6436650
Kanatani, S. et al. The COUP-TFII/Neuropilin-2 is a molecular switch steering diencephalon-derived GABAergic neurons in the developing mouse brain. Proc. Natl Acad. Sci. USA 112, E4985–E4994 (2015).
doi: 10.1073/pnas.1420701112
pubmed: 26305926
pmcid: 4568674
Corona, C. et al. Activating transcription factor 4 (ATF4) regulates neuronal activity by controlling GABABR trafficking. J. Neurosci. 38, 6102–6113 (2018).
doi: 10.1523/JNEUROSCI.3350-17.2018
pubmed: 29875265
pmcid: 6596153
Shinghal, R., Scheller, R. H. & Bajjalieh, S. M. Ceramide 1-phosphate phosphatase activity in brain. J. Neurochem. 61, 2279–2285 (1993).
doi: 10.1111/j.1471-4159.1993.tb07470.x
pubmed: 8245978
Oegema, R. et al. Human mutations in integrator complex subunits link transcriptome integrity to brain development. PLoS Genet. 13, e1006809 (2017).
doi: 10.1371/journal.pgen.1006809
pubmed: 28542170
pmcid: 5466333
Hamley, I. W. The amyloid beta peptide: a chemist’s perspective. Role in Alzheimer’s and fibrillization. Chem. Rev. 112, 5147–5192 (2012).
doi: 10.1021/cr3000994
pubmed: 22813427
Wang, Q., Moore, M. J., Adelmant, G., Marto, J. A. & Silver, P. A. PQBP1, a factor linked to intellectual disability, affects alternative splicing associated with neurite outgrowth. Genes Dev. 27, 615–626 (2013).
doi: 10.1101/gad.212308.112
pubmed: 23512658
pmcid: 3613609
Zadjali, F. et al. Homozygosity for FARSB mutation leads to Phe-tRNA synthetase-related disease of growth restriction, brain calcification, and interstitial lung disease. Hum. Mutat. 39, 1355–1359 (2018).
doi: 10.1002/humu.23595
pubmed: 30014610
Fiorito, G. et al. Guidelines for the care and welfare of cephalopods in research—a consensus based on an initiative by CephRes, FELASA and the Boyd Group. Lab. Anim. 49, 1–90 (2015).
doi: 10.1177/0023677215580006
pubmed: 26354955
Butler-Struben, H. M., Brophy, S. M., Johnson, N. A. & Crook, R. J. In vivo recording of neural and behavioral correlates of anesthesia induction, reversal, and euthanasia in cephalopod molluscs. Front. Physiol. 9, 109 (2018).
Shigeno, S., Parnaik, R., Albertin, C. B. & Ragsdale, C. W. Evidence for a cordal, not ganglionic, pattern of cephalopod brain neurogenesis. Zoological Lett. https://doi.org/10.1186/s40851-015-0026-z (2015).
Collins, A. J. & Nyholm, S. V. Obtaining hemocytes from the Hawaiian bobtail squid Euprymna scolopes and observing their adherence to symbiotic and non-symbiotic bacteria. J. Vis. Exp. JoVE 1714, https://doi.org/10.3791/1714 (2010).
Lee, P. N., Callaerts, P. & de Couet, H. G. The embryonic development of the Hawaiian bobtail squid (Euprymna scolopes). Cold Spring Harb. Protoc. 2009, pdb.ip77 (2009).
doi: 10.1101/pdb.ip77
pubmed: 20150049
Rao, S. S. P. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665–1680 (2014).
doi: 10.1016/j.cell.2014.11.021
pubmed: 25497547
pmcid: 5635824
Serra, F. et al. Automatic analysis and 3D-modelling of Hi-C data using TADbit reveals structural features of the fly chromatin colors. PLOS Comput. Biol. 13, e1005665 (2017).
doi: 10.1371/journal.pcbi.1005665
pubmed: 28723903
pmcid: 5540598
Wolff, J. et al. Galaxy HiCExplorer 3: a web server for reproducible Hi-C, capture Hi-C and single-cell Hi-C data analysis, quality control and visualization. Nucleic Acids Res. https://doi.org/10.1093/nar/gkaa220 (2020).
Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinforma. 10, 421 (2009).
doi: 10.1186/1471-2105-10-421
Engström, P. G., Fredman, D. & Lenhard, B. Ancora: a web resource for exploring highly conserved noncoding elements and their association with developmental regulatory genes. Genome Biol. 9, R34 (2008).
doi: 10.1186/gb-2008-9-2-r34
pubmed: 18279518
pmcid: 2374709
Bejerano, G. et al. Ultraconserved elements in the human genome. Science 304, 1321–1325 (2004).
doi: 10.1126/science.1098119
pubmed: 15131266
Neph, S. et al. BEDOPS: high-performance genomic feature operations. Bioinformatics 28, 1919–1920 (2012).
doi: 10.1093/bioinformatics/bts277
pubmed: 22576172
pmcid: 3389768
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
doi: 10.1093/bioinformatics/btq033
pubmed: 20110278
pmcid: 2832824
Bailey, T. L., Johnson, J., Grant, C. E. & Noble, W. S. The MEME suite. Nucleic Acids Res. 43, W39–W49 (2015).
doi: 10.1093/nar/gkv416
pubmed: 25953851
pmcid: 4489269
Sayers, E. W. et al. Database resources of the national center for biotechnology information. Nucleic Acids Res. 50, D20–D26 (2022).
doi: 10.1093/nar/gkab1112
pubmed: 34850941
Corces, M. R. et al. An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues. Nat. Methods 14, 959–962 (2017).
doi: 10.1038/nmeth.4396
pubmed: 28846090
pmcid: 5623106
Buenrostro et al. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. Ed. Frederick M Ausubel Al 109, 21.29.1–21.29.9 (2015).
Tanner, A. R. et al. Molecular clocks indicate turnover and diversification of modern coleoid cephalopods during the Mesozoic Marine Revolution. Proc. R. Soc. B Biol. Sci. 284, 20162818 (2017).
doi: 10.1098/rspb.2016.2818
Kröger, B., Vinther, J. & Fuchs, D. Cephalopod origin and evolution: a congruent picture emerging from fossils, development and molecules. BioEssays 33, 602–613 (2011).
doi: 10.1002/bies.201100001
pubmed: 21681989