publication . Article . 2018

Amphioxus functional genomics and the origins of vertebrate gene regulation

Ferdinand Marlétaz; Panos N Firbas; Ignacio Maeso; Juan J. Tena; Ozren Bogdanovic; Malcolm Perry; Christopher D. R. Wyatt; Elisa de la Calle-Mustienes; Stéphanie Bertrand; Demian Burguera; ...
Open Access
  • Published: 05 Dec 2018
Abstract
This research was funded primarily by the European Research Council (ERC) under the European Union’s Horizon 2020 and Seventh Framework Program FP7 research and innovation programs (ERC-AdG-LS8-740041 to J.L.G.-S., ERC-StG-LS2-637591 to M.I., a Marie Sklodowska-Curie Grant (658521) to I.M. and a FP7/2007-2013-ERC-268513 to P.W.H.H.), the Spanish Ministerio de Economía y Competitividad (BFU2016-74961-P to J.L.G.-S., RYC-2016-20089 to I.M., BFU2014-55076-P and BFU2017-89201-P to M.I. and BFU2014-55738-REDT to J.L.G.-S, M.I. and J.R.M.-M), the ‘Centro de Excelencia Severo Ochoa 2013-2017’(SEV-2012-0208), the ‘Unidad de Excelencia María de Maetzu 2017-2021’(MDM-2016...
Subjects
free text keywords: [SDV.MHEP.MI]Life Sciences [q-bio]/Human health and pathology/Infectious diseases, Epigenomics, Functional genomics, Molecular evolution, Animals, Vertebrates, Humans, Genomics, DNA Methylation, Gene Expression Regulation, Body Patterning, Promoter Regions, Genetic, Molecular Sequence Annotation, Transcriptome, Lancelets, Animals, Vertebrates, Humans, Genomics, DNA Methylation, Gene Expression Regulation, Body Patterning, Promoter Regions, Genetic, Molecular Sequence Annotation, Transcriptome, Lancelets, [SDV.BDD.EO]Life Sciences [q-bio]/Development Biology/Embryology and Organogenesis, Article, whole genome duplication, regulatory genomics, transcriptomics, DDC model, hourglass model, chordate evolution, Multidisciplinary, Epigenomics, Functional genomics, Molecular evolution, Science & Technology, Multidisciplinary Sciences, Science & Technology - Other Topics, BRANCHIOSTOMA-LANCEOLATUM, DNA DEMETHYLATION, CHROMATIN, EVOLUTION, SEQ, CONSERVATION, LANDSCAPES, ZEBRAFISH, PLURIPOTENCY, TRANSGENESIS, General Science & Technology, comparative study, developmental stage, evolution, gene, gene expression, genetic analysis, innovation, invertebrate, specialization, vertebrate, adult, animal cell, animal tissue, Article, Branchiostoma, chromatin, controlled study, embryo, embryo development, female, gene control, gene duplication, gene sequence, genome, histone modification, male, molecular genetics, mouse, multigene family, nonhuman, priority journal, zebra fish, Branchiostoma lanceolatum, Vertebrata, Vertebrats, Amfiox, Amphioxus, Ancestral Expression, Whole-genome Duplication (WGD), Phylotypic Period, Branchiostoma Lanceolatum, QH426 Genetics, DAS, QH426, Gene duplication, Genome, Subfunctionalization, Genomics, Vertebrate, biology.animal, biology, Regulation of gene expression, Branchiostoma, biology.organism_classification, Evolutionary biology, Functional genomics
Communities
Communities with gateway
OpenAIRE Connect image
Funded by
EC| EVOREL
Project
EVOREL
Evolution of Regulatory Landscapes in Chordates
  • Funder: European Commission (EC)
  • Project Code: 658521
  • Funding stream: H2020 | MSCA-IF-EF-ST
,
EC| BLUEandGREEN
Project
BLUEandGREEN
Boosting scientific excellence and innovation capacity in biorefineries based on marine resources
  • Funder: European Commission (EC)
  • Project Code: 692419
  • Funding stream: H2020 | CSA
Validated by funder
,
EC| Evoland
Project
Evoland
Evolution of regulatory landscapes at multiple timescales
  • Funder: European Commission (EC)
  • Project Code: 740041
  • Funding stream: H2020 | ERC | ERC-ADG
Validated by funder
,
EC| NEURAL AS
Project
NEURAL AS
Functions and evolutionary impact of transcriptomic novelties in the vertebrate brain
  • Funder: European Commission (EC)
  • Project Code: 637591
  • Funding stream: H2020 | ERC | ERC-STG
Validated by funder
,
EC| DEVCOM
Project
DEVCOM
European Initial Training Network on Developmental and Computational Biology
  • Funder: European Commission (EC)
  • Project Code: 607142
  • Funding stream: FP7 | SP3 | PEOPLE
73 references, page 1 of 5

1. Bertrand, S. & Escriva, H. Evolutionary crossroads in developmental biology: amphioxus. Development 138, 4819-4830 (2011).

2. Dehal, P. & Boore, J. L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314 (2005). [OpenAIRE]

3. Putnam, N. H. et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064-1071 (2008).

4. Holland, L. Z. et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 18, 1100-1111 (2008).

5. International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).

6. Nelson, C. E., Hersh, B. M. & Carroll, S. B. The regulatory content of intergenic DNA shapes genome architecture. Genome Biol. 5, R25 (2004).

7. Bogdanović, O. et al. Active DNA demethylation at enhancers during the vertebrate phylotypic period. Nat. Genet. 48, 417-426 (2016).

8. Berthelot, C., Villar, D., Horvath, J. E., Odom, D. T. & Flicek, P. Complexity and conservation of regulatory landscapes underlie evolutionary resilience of mammalian gene expression. Nat. Ecol. Evol. 2, 152-163 (2018).

9. Reilly, S. K. et al. Evolutionary changes in promoter and enhancer activity during human corticogenesis. Science 347, 1155-1159 (2015).

10. Villar, D. et al. Enhancer evolution across 20 mammalian species. Cell 160, 554-566 (2015). [OpenAIRE]

11. Vierstra, J. et al. Mouse regulatory DNA landscapes reveal global principles of cis-regulatory evolution. Science 346, 1007-1012 (2014).

12. Boyle, A. P. et al. Comparative analysis of regulatory information and circuits across distant species. Nature 512, 453-456 (2014).

13. Gerstein, M. B. et al. Comparative analysis of the transcriptome across distant species. Nature 512, 445-448 (2014).

14. Hendrich, B. & Tweedie, S. The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 19, 269-277 (2003). [OpenAIRE]

15. Irimia, M. et al. Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints. Genome Res. 22, 2356-2367 (2012).

73 references, page 1 of 5
Abstract
This research was funded primarily by the European Research Council (ERC) under the European Union’s Horizon 2020 and Seventh Framework Program FP7 research and innovation programs (ERC-AdG-LS8-740041 to J.L.G.-S., ERC-StG-LS2-637591 to M.I., a Marie Sklodowska-Curie Grant (658521) to I.M. and a FP7/2007-2013-ERC-268513 to P.W.H.H.), the Spanish Ministerio de Economía y Competitividad (BFU2016-74961-P to J.L.G.-S., RYC-2016-20089 to I.M., BFU2014-55076-P and BFU2017-89201-P to M.I. and BFU2014-55738-REDT to J.L.G.-S, M.I. and J.R.M.-M), the ‘Centro de Excelencia Severo Ochoa 2013-2017’(SEV-2012-0208), the ‘Unidad de Excelencia María de Maetzu 2017-2021’(MDM-2016...
Subjects
free text keywords: [SDV.MHEP.MI]Life Sciences [q-bio]/Human health and pathology/Infectious diseases, Epigenomics, Functional genomics, Molecular evolution, Animals, Vertebrates, Humans, Genomics, DNA Methylation, Gene Expression Regulation, Body Patterning, Promoter Regions, Genetic, Molecular Sequence Annotation, Transcriptome, Lancelets, Animals, Vertebrates, Humans, Genomics, DNA Methylation, Gene Expression Regulation, Body Patterning, Promoter Regions, Genetic, Molecular Sequence Annotation, Transcriptome, Lancelets, [SDV.BDD.EO]Life Sciences [q-bio]/Development Biology/Embryology and Organogenesis, Article, whole genome duplication, regulatory genomics, transcriptomics, DDC model, hourglass model, chordate evolution, Multidisciplinary, Epigenomics, Functional genomics, Molecular evolution, Science & Technology, Multidisciplinary Sciences, Science & Technology - Other Topics, BRANCHIOSTOMA-LANCEOLATUM, DNA DEMETHYLATION, CHROMATIN, EVOLUTION, SEQ, CONSERVATION, LANDSCAPES, ZEBRAFISH, PLURIPOTENCY, TRANSGENESIS, General Science & Technology, comparative study, developmental stage, evolution, gene, gene expression, genetic analysis, innovation, invertebrate, specialization, vertebrate, adult, animal cell, animal tissue, Article, Branchiostoma, chromatin, controlled study, embryo, embryo development, female, gene control, gene duplication, gene sequence, genome, histone modification, male, molecular genetics, mouse, multigene family, nonhuman, priority journal, zebra fish, Branchiostoma lanceolatum, Vertebrata, Vertebrats, Amfiox, Amphioxus, Ancestral Expression, Whole-genome Duplication (WGD), Phylotypic Period, Branchiostoma Lanceolatum, QH426 Genetics, DAS, QH426, Gene duplication, Genome, Subfunctionalization, Genomics, Vertebrate, biology.animal, biology, Regulation of gene expression, Branchiostoma, biology.organism_classification, Evolutionary biology, Functional genomics
Communities
Communities with gateway
OpenAIRE Connect image
Funded by
EC| EVOREL
Project
EVOREL
Evolution of Regulatory Landscapes in Chordates
  • Funder: European Commission (EC)
  • Project Code: 658521
  • Funding stream: H2020 | MSCA-IF-EF-ST
,
EC| BLUEandGREEN
Project
BLUEandGREEN
Boosting scientific excellence and innovation capacity in biorefineries based on marine resources
  • Funder: European Commission (EC)
  • Project Code: 692419
  • Funding stream: H2020 | CSA
Validated by funder
,
EC| Evoland
Project
Evoland
Evolution of regulatory landscapes at multiple timescales
  • Funder: European Commission (EC)
  • Project Code: 740041
  • Funding stream: H2020 | ERC | ERC-ADG
Validated by funder
,
EC| NEURAL AS
Project
NEURAL AS
Functions and evolutionary impact of transcriptomic novelties in the vertebrate brain
  • Funder: European Commission (EC)
  • Project Code: 637591
  • Funding stream: H2020 | ERC | ERC-STG
Validated by funder
,
EC| DEVCOM
Project
DEVCOM
European Initial Training Network on Developmental and Computational Biology
  • Funder: European Commission (EC)
  • Project Code: 607142
  • Funding stream: FP7 | SP3 | PEOPLE
73 references, page 1 of 5

1. Bertrand, S. & Escriva, H. Evolutionary crossroads in developmental biology: amphioxus. Development 138, 4819-4830 (2011).

2. Dehal, P. & Boore, J. L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314 (2005). [OpenAIRE]

3. Putnam, N. H. et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064-1071 (2008).

4. Holland, L. Z. et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 18, 1100-1111 (2008).

5. International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).

6. Nelson, C. E., Hersh, B. M. & Carroll, S. B. The regulatory content of intergenic DNA shapes genome architecture. Genome Biol. 5, R25 (2004).

7. Bogdanović, O. et al. Active DNA demethylation at enhancers during the vertebrate phylotypic period. Nat. Genet. 48, 417-426 (2016).

8. Berthelot, C., Villar, D., Horvath, J. E., Odom, D. T. & Flicek, P. Complexity and conservation of regulatory landscapes underlie evolutionary resilience of mammalian gene expression. Nat. Ecol. Evol. 2, 152-163 (2018).

9. Reilly, S. K. et al. Evolutionary changes in promoter and enhancer activity during human corticogenesis. Science 347, 1155-1159 (2015).

10. Villar, D. et al. Enhancer evolution across 20 mammalian species. Cell 160, 554-566 (2015). [OpenAIRE]

11. Vierstra, J. et al. Mouse regulatory DNA landscapes reveal global principles of cis-regulatory evolution. Science 346, 1007-1012 (2014).

12. Boyle, A. P. et al. Comparative analysis of regulatory information and circuits across distant species. Nature 512, 453-456 (2014).

13. Gerstein, M. B. et al. Comparative analysis of the transcriptome across distant species. Nature 512, 445-448 (2014).

14. Hendrich, B. & Tweedie, S. The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 19, 269-277 (2003). [OpenAIRE]

15. Irimia, M. et al. Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints. Genome Res. 22, 2356-2367 (2012).

73 references, page 1 of 5
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