Emx2 underlies the development and evolution of marsupial gliding membranes.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
24 Apr 2024
24 Apr 2024
Historique:
received:
28
03
2023
accepted:
13
03
2024
medline:
25
4
2024
pubmed:
25
4
2024
entrez:
24
4
2024
Statut:
aheadofprint
Résumé
Phenotypic variation among species is a product of evolutionary changes to developmental programs
Identifiants
pubmed: 38658750
doi: 10.1038/s41586-024-07305-3
pii: 10.1038/s41586-024-07305-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Carroll, S. B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25–36 (2008).
pubmed: 18614008
doi: 10.1016/j.cell.2008.06.030
Stern, D. L. Evolutionary developmental biology and the problem of variation. Evolution 54, 1079–1091 (2000).
pubmed: 11005278
Davidson, E. H. & Erwin, D. H. Gene regulatory networks and the evolution of animal body plans. Science 311, 796–800 (2006).
pubmed: 16469913
doi: 10.1126/science.1113832
Wittkopp, P. J. & Kalay, G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat. Rev. Genet. 13, 59–69 (2012).
doi: 10.1038/nrg3095
Zhen, Y., Aardema, M. L., Medina, E. M., Schumer, M. & Andolfatto, P. Parallel molecular evolution in an herbivore community. Science 337, 1634–1637 (2012).
pubmed: 23019645
pmcid: 3770729
doi: 10.1126/science.1226630
Chan, Y. F. et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302–305 (2010).
pubmed: 20007865
doi: 10.1126/science.1182213
Manceau, M., Domingues, V. S., Linnen, C. R., Rosenblum, E. B. & Hoekstra, H. E. Convergence in pigmentation at multiple levels: mutations, genes and function. Philos. Trans. R. Soc. Lond. B 365, 2439–2450 (2010).
Losos, J. B. Convergence, adaptation, and constraint. Evolution 65, 1827–1840 (2011).
pubmed: 21729041
doi: 10.1111/j.1558-5646.2011.01289.x
Stern, D. L. The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751–764 (2013).
pubmed: 24105273
doi: 10.1038/nrg3483
Storz, J. F. Causes of molecular convergence and parallelism in protein evolution. Nat. Rev. Genet. 17, 239–250 (2016).
pubmed: 26972590
pmcid: 5482790
doi: 10.1038/nrg.2016.11
Goldingay, R. L. & Scheibe, J. S. Biology of Gliding Mammals (Filander, 2000).
Lindenmayer, D. Gliders of Australia (UNSW Press, 2002).
May-Collado, L. J., Kilpatrick, C. W. & Agnarsson, I. Mammals from “down under”: a multi-gene species-level phylogeny of marsupial mammals (Mammalia, Metatheria). PeerJ 3, e805 (2015).
pubmed: 25755933
pmcid: 4349131
doi: 10.7717/peerj.805
Feigin, C. Y. et al. Convergent deployment of ancestral functions during the evolution of mammalian flight membranes. Sci. Adv. 9, eade7511 (2023).
pubmed: 36961889
pmcid: 10038344
doi: 10.1126/sciadv.ade7511
Hubisz, M. J. & Pollard, K. S. Exploring the genesis and functions of human accelerated regions sheds light on their role in human evolution. Curr. Opin. Genet. Dev. 29, 15–21 (2014).
pubmed: 25156517
doi: 10.1016/j.gde.2014.07.005
Booker, B. M. et al. Bat accelerated regions identify a bat forelimb specific enhancer in the HoxD locus. PLoS Genet. 12, e1005738 (2016).
pubmed: 27019019
pmcid: 4809552
doi: 10.1371/journal.pgen.1005738
Whalen, S. & Pollard, K. S. Enhancer function and evolutionary roles of human accelerated regions. Annu. Rev. Genet. 56, 423–439 (2022).
pubmed: 36070559
pmcid: 9712246
doi: 10.1146/annurev-genet-071819-103933
Dudchenko, O. et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92–95 (2017).
pubmed: 28336562
pmcid: 5635820
doi: 10.1126/science.aal3327
Manni, M., Berkeley, M. R., Seppey, M., Simão, F. A. & Zdobnov, E. M. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol. Biol. Evol. 38, 4647–4654 (2021).
pubmed: 34320186
pmcid: 8476166
doi: 10.1093/molbev/msab199
Buenrostro, J. D., Wu, B., Chang, H. Y. & Greenleaf, W. J. ATAC‐seq: a method for assaying chromatin accessibility genome‐wide. Curr. Protoc. Mol. Biol. 109, 21.29.1–21.29.9 (2015).
pubmed: 25559105
doi: 10.1002/0471142727.mb2129s109
Creyghton, M. P. et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl Acad. Sci. USA 107, 21931–21936 (2010).
Cherry, T. J. et al. Mapping the cis-regulatory architecture of the human retina reveals noncoding genetic variation in disease. Proc. Natl Acad. Sci. USA 117, 9001–9012 (2020).
pubmed: 32265282
pmcid: 7183164
doi: 10.1073/pnas.1922501117
Hoencamp, C. et al. 3D genomics across the tree of life reveals condensin II as a determinant of architecture type. Science 372, 984–989 (2021).
pubmed: 34045355
pmcid: 8172041
doi: 10.1126/science.abe2218
Johnson, R. N. et al. Adaptation and conservation insights from the koala genome. Nat. Genet. 50, 1102–1111 (2018).
pubmed: 29967444
pmcid: 6197426
doi: 10.1038/s41588-018-0153-5
Pollard, K. S., Hubisz, M. J., Rosenbloom, K. R. & Siepel, A. Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res. 20, 110–121 (2010).
pubmed: 19858363
pmcid: 2798823
doi: 10.1101/gr.097857.109
Villar, D. et al. Enhancer evolution across 20 mammalian species. Cell 160, 554–566 (2015).
pubmed: 25635462
pmcid: 4313353
doi: 10.1016/j.cell.2015.01.006
Hsieh, T.-H. S. et al. Mapping nucleosome resolution chromosome folding in yeast by Micro-C. Cell 162, 108–119 (2015).
pubmed: 26119342
pmcid: 4509605
doi: 10.1016/j.cell.2015.05.048
Grant, C. E. & Bailey, T. L. XSTREME: Comprehensive motif analysis of biological sequence datasets. Preprint at bioRxiv https://doi.org/10.1101/2021.09.02.458722 (2021).
Miyamoto, N., Yoshida, M., Kuratani, S., Matsuo, I. & Aizawa, S. Defects of urogenital development in mice lacking Emx2. Development 124, 1653–1664 (1997).
pubmed: 9165114
doi: 10.1242/dev.124.9.1653
Mallamaci, A. et al. EMX2 protein in the developing mouse brain and olfactory area. Mech. Dev. 77, 165–172 (1998).
pubmed: 9831645
doi: 10.1016/S0925-4773(98)00141-5
Cecchi, C. & Boncinelli, E. Emx homeogenes and mouse brain development. Trends Neurosci. 23, 347–352 (2000).
pubmed: 10906797
doi: 10.1016/S0166-2236(00)01608-8
Pellegrini, M., Pantano, S., Fumi, M. P., Lucchini, F. & Forabosco, A. Agenesis of the scapula in Emx2 homozygous mutants. Dev. Biol. 232, 149–156 (2001).
pubmed: 11254354
doi: 10.1006/dbio.2001.0159
Capellini, T. D. et al. Control of pelvic girdle development by genes of the Pbx family and Emx2. Dev. Dyn. 240, 1173–1189 (2011).
pubmed: 21455939
pmcid: 3081414
doi: 10.1002/dvdy.22617
Beronja, S., Livshits, G., Williams, S. & Fuchs, E. Rapid functional dissection of genetic networks via tissue-specific transduction and RNAi in mouse embryos. Nat. Med. 16, 821–827 (2010).
pubmed: 20526348
pmcid: 2911018
doi: 10.1038/nm.2167
Muzio, L., Soria, J. M., Pannese, M., Piccolo, S. & Mallamaci, A. A mutually stimulating loop involving emx2 and canonical wnt signalling specifically promotes expansion of occipital cortex and hippocampus. Cereb. Cortex 15, 2021–2028 (2005).
pubmed: 15800025
doi: 10.1093/cercor/bhi077
Bailey, T. L. STREME: accurate and versatile sequence motif discovery. Bioinformatics 37, 2834–2840 (2021).
pubmed: 33760053
pmcid: 8479671
doi: 10.1093/bioinformatics/btab203
Grant, C. E., Bailey, T. L. & Noble, W. S. FIMO: scanning for occurrences of a given motif. Bioinformatics 27, 1017–1018 (2011).
pubmed: 21330290
pmcid: 3065696
doi: 10.1093/bioinformatics/btr064
Szklarczyk, D. et al. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, D607–D613 (2018).
pmcid: 6323986
doi: 10.1093/nar/gky1131
Stephens, T. D. The Wolffian ridge: history of a misconception. ISIS 73, 254–259 (1982).
pubmed: 7050012
doi: 10.1086/352972
Rezza, A. et al. Signaling networks among stem cell precursors, transit-amplifying progenitors, and their niche in developing hair follicles. Cell Rep. 14, 3001–3018 (2016).
pubmed: 27009580
pmcid: 4826467
doi: 10.1016/j.celrep.2016.02.078
Sennett, R. et al. An integrated transcriptome atlas of embryonic hair follicle progenitors, their niche, and the developing skin. Dev. Cell 34, 577–591 (2015).
pubmed: 26256211
pmcid: 4573840
doi: 10.1016/j.devcel.2015.06.023
Jiang, T., Kindt, K. & Wu, D. K. Transcription factor Emx2 controls stereociliary bundle orientation of sensory hair cells. eLife 6, e23661 (2017).
pubmed: 28266911
pmcid: 5388538
doi: 10.7554/eLife.23661
Chung, M.-I., Bujnis, M., Barkauskas, C. E., Kobayashi, Y. & Hogan, B. L. M. Niche-mediated BMP/SMAD signaling regulates lung alveolar stem cell proliferation and differentiation. Development 145, dev163014 (2018).
pubmed: 29752282
pmcid: 5992594
doi: 10.1242/dev.163014
Osterwalder, M. et al. in Craniofacial Development: Methods and Protocols (ed. Dworkin, S.) 147–186 (Springer, 2022).
Dalton, D., Chadwick, R. & McGinnis, W. Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev. 3, 1940–1956 (1989).
pubmed: 2576012
doi: 10.1101/gad.3.12a.1940
Kimura, J. et al. Emx2 and Pax6 function in cooperation with Otx2 and Otx1 to develop caudal forebrain primordium that includes future archipallium. J. Neurosci. 25, 5097–5108 (2005).
pubmed: 15917450
pmcid: 6724811
doi: 10.1523/JNEUROSCI.0239-05.2005
Cohen, S. M. & Jürgens, G. Mediation of Drosophila head development by gap-like segmentation genes. Nature 346, 482–485 (1990).
pubmed: 1974035
doi: 10.1038/346482a0
Feigin, C. Y., Newton, A. H. & Pask, A. J. Widespread cis-regulatory convergence between the extinct Tasmanian tiger and gray wolf. Genome Res. 29, 1648–1658 (2019).
pubmed: 31533979
pmcid: 6771401
doi: 10.1101/gr.244251.118
Dudchenko, O. et al. The Juicebox Assembly Tools module facilitates de novo assembly of mammalian genomes with chromosome-length scaffolds for under $1000. Preprint at bioRxiv https://doi.org/10.1101/254797 (2018).
Li, D., Liu, C.-M., Luo, R., Sadakane, K. & Lam, T.-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015).
pubmed: 25609793
doi: 10.1093/bioinformatics/btv033
Pryszcz, L. P. & Gabaldón, T. Redundans: an assembly pipeline for highly heterozygous genomes. Nucleic Acids Res. 44, e113 (2016).
pubmed: 27131372
pmcid: 4937319
doi: 10.1093/nar/gkw294
Alonge, M. et al. RaGOO: fast and accurate reference-guided scaffolding of draft genomes. Genome Biol. 20, 224 (2019).
pubmed: 31661016
pmcid: 6816165
doi: 10.1186/s13059-019-1829-6
Corces, M. R. et al. An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues. Nat. Methods 14, 959–962 (2017).
pubmed: 28846090
pmcid: 5623106
doi: 10.1038/nmeth.4396
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286
pmcid: 3322381
doi: 10.1038/nmeth.1923
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
pubmed: 18798982
pmcid: 2592715
doi: 10.1186/gb-2008-9-9-r137
Li, Q., Brown, J. B., Huang, H. & Bickel, P. J. Measuring reproducibility of high-throughput experiments. Ann. Appl. Stat. 5, 1752–1779 (2011).
doi: 10.1214/11-AOAS466
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278
pmcid: 2832824
doi: 10.1093/bioinformatics/btq033
Bailey, T. L. & Grant, C. E. SEA: simple enrichment analysis of motifs. Preprint at bioRxiv https://doi.org/10.1101/2021.08.23.457422 (2021).
Bailey, T. L., Johnson, J., Grant, C. E. & Noble, W. S. The MEME suite. Nucleic Acids Res. 43, W39–W49 (2015).
pubmed: 25953851
pmcid: 4489269
doi: 10.1093/nar/gkv416
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Hubisz, M. J., Pollard, K. S. & Siepel, A. PHAST and RPHAST: phylogenetic analysis with space/time models. Brief. Bioinform. 12, 41–51 (2011).
pubmed: 21278375
doi: 10.1093/bib/bbq072
Langschied, F., Leisegang, M. S., Brandes, R. P. & Ebersberger, I. ncOrtho: efficient and reliable identification of miRNA orthologs. Nucleic Acids Res. 51, e71 (2023).
pubmed: 37260093
pmcid: 10359484
doi: 10.1093/nar/gkad467
Pertea, G. & Pertea, M. GFF utilities: GffRead and GffCompare. F1000Res. 9, J-304 (2020).
Sackton, T. B. et al. Convergent regulatory evolution and loss of flight in paleognathous birds. Science 364, 74–78 (2019).
pubmed: 30948549
doi: 10.1126/science.aat7244
Jarvis, E. D. et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346, 1320–1331 (2014).
pubmed: 25504713
pmcid: 4405904
doi: 10.1126/science.1253451
Meredith, R. W., Westerman, M. & Springer, M. S. A phylogeny of Diprotodontia (Marsupialia) based on sequences for five nuclear genes. Mol. Phylogenet. Evol. 51, 554–571 (2009).
pubmed: 19249373
doi: 10.1016/j.ympev.2009.02.009
Doronina, L., Feigin, C. Y. & Schmitz, J. Reunion of Australasian possums by shared SINE insertions. Syst. Biol. 71, 1045–1053 (2022).
pubmed: 35289914
pmcid: 9366447
doi: 10.1093/sysbio/syac025
Long, H. S. et al. Making sense of the linear genome, gene function and TADs. Epigenet. Chromatin 15, 4 (2022).
doi: 10.1186/s13072-022-00436-9
Kent, W. J. BLAT—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).
pubmed: 11932250
pmcid: 187518
Kent, W. J. et al. The Human Genome Browser at UCSC. Genome Res. 12, 996–1006 (2002).
pubmed: 12045153
pmcid: 186604
doi: 10.1101/gr.229102
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
pubmed: 2231712
doi: 10.1016/S0022-2836(05)80360-2
Kuleshov, M. V. et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 44, W90–W97 (2016).
pubmed: 27141961
pmcid: 4987924
doi: 10.1093/nar/gkw377
Gupta, S., Stamatoyannopoulos, J. A., Bailey, T. L. & Noble, W. S. Quantifying similarity between motifs. Genome Biol. 8, R24 (2007).
pubmed: 17324271
pmcid: 1852410
doi: 10.1186/gb-2007-8-2-r24
Johnson, M. R. et al. A multifunctional Wnt regulator underlies the evolution of rodent stripe patterns. Nat. Ecol. Evol. 7, 2143–2159 (2023).
pubmed: 37813945
pmcid: 10839778
doi: 10.1038/s41559-023-02213-7
Hao, Y. et al. Dictionary learning for integrative, multimodal and scalable single-cell analysis. Nat. Biotechnol. 42, 293–304 (2023).
pubmed: 37231261
pmcid: 10928517
doi: 10.1038/s41587-023-01767-y
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
Durand, N. C. et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 3, 95–98 (2016).
pubmed: 27467249
pmcid: 5846465
doi: 10.1016/j.cels.2016.07.002
Roayaei Ardakany, A., Gezer, H. T., Lonardi, S. & Ay, F. Mustache: multi-scale detection of chromatin loops from Hi-C and Micro-C maps using scale-space representation. Genome Biol. 21, 256 (2020).
pubmed: 32998764
pmcid: 7528378
doi: 10.1186/s13059-020-02167-0
Kerpedjiev, P. et al. HiGlass: web-based visual exploration and analysis of genome interaction maps. Genome Biol. 19, 125 (2018).
pubmed: 30143029
pmcid: 6109259
doi: 10.1186/s13059-018-1486-1
Abdennur, N. & Mirny, L. A. Cooler: scalable storage for Hi-C data and other genomically labeled arrays. Bioinformatics 36, 311–316 (2020).
pubmed: 31290943
doi: 10.1093/bioinformatics/btz540
Aasen, T. & Izpisúa Belmonte, J. C. Isolation and cultivation of human keratinocytes from skin or plucked hair for the generation of induced pluripotent stem cells. Nat. Protoc. 5, 371–382 (2010).
pubmed: 20134422
doi: 10.1038/nprot.2009.241
Moffat, J. et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed airal high-content screen. Cell 124, 1283–1298 (2006).
pubmed: 16564017
doi: 10.1016/j.cell.2006.01.040
Mallarino, R. et al. Developmental mechanisms of stripe patterns in rodents. Nature 539, 518–523 (2016).
pubmed: 27806375
pmcid: 5292240
doi: 10.1038/nature20109
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2013).
pubmed: 24227677
doi: 10.1093/bioinformatics/btt656
Wu, J. & Wang, X. Whole-mount in situ hybridization of mouse embryos using DIG-labeled RNA probes. Methods Mol. Biol. 1922, 151–159 (2019).
pubmed: 30838573
doi: 10.1007/978-1-4939-9012-2_15
Chen, A. et al. Spatiotemporal transcriptomic atlas of mouse organogenesis using DNA nanoball-patterned arrays. Cell 185, 1777–1792 (2022).
pubmed: 35512705
doi: 10.1016/j.cell.2022.04.003
Ren, H., Walker, B. L., Cang, Z. & Nie, Q. Identifying multicellular spatiotemporal organization of cells with SpaceFlow. Nat. Commun. 13, 4076 (2022).
pubmed: 35835774
pmcid: 9283532
doi: 10.1038/s41467-022-31739-w
van Amerongen, R., Fuerer, C., Mizutani, M. & Nusse, R. Wnt5a can both activate and repress Wnt/β-catenin signaling during mouse embryonic development. Dev. Biol. 369, 101–114 (2012).
pubmed: 22771246
pmcid: 3435145
doi: 10.1016/j.ydbio.2012.06.020
Hochedlinger, K., Yamada, Y., Beard, C. & Jaenisch, R. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 121, 465–477 (2005).
pubmed: 15882627
doi: 10.1016/j.cell.2005.02.018
Kvon, E. Z. et al. Comprehensive in vivo interrogation reveals phenotypic impact of human enhancer variants. Cell 180, 1262–1271 (2020).
pubmed: 32169219
pmcid: 7179509
doi: 10.1016/j.cell.2020.02.031
Moreno, J. A. et al. Emx2 underlies the development and evolution of marsupial gliding membranes. FigShare figshare.com/s/81cf39b7de363f1526a1 (2024).