Modularity and hierarchy in biological systems: Using gene regulatory networks to understand evolutionary change

Current Topics in Developmental Biology - Tập 141 - Trang 39-73 - 2021
William L. Hatleberg1, Veronica F. Hinman1
1Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA, United States

Tài liệu tham khảo

Abzhanov, 2013, von Baer's law for the ages: Lost and found principles of developmental evolution, Trends in Genetics, 29, 712, 10.1016/j.tig.2013.09.004 Akam, 1998, Hox genes, homeosis and the evolution of segment identity: No need for hopeless monsters, The International Journal of Developmental Biology, 42, 445 Amore, 2010, Size matters: The contribution of cell proliferation to the progression of the specification Drosophila eye gene regulatory network, Developmental Biology, 344, 569, 10.1016/j.ydbio.2010.06.015 Aragona, 2020, Mechanisms of stretch-mediated skin expansion at single-cell resolution, Nature, 584, 268, 10.1038/s41586-020-2555-7 Arendt, 2001, Evolution of the bilaterian larval foregut, Nature, 409, 81, 10.1038/35051075 Arnone, 2015, Echinodermata, vol. 6, 1 Arnosti, 2005, Transcriptional enhancers: Intelligent enhanceosomes or flexible billboards?, Journal of Cellular Biochemistry, 94, 890, 10.1002/jcb.20352 Badis, 2009, Diversity and complexity in DNA recognition by transcription factors, Science, 324, 1720, 10.1126/science.1162327 Ben-Tabou De-Leon, 2007, Gene regulation: Gene control network in development, Annual Review of Biophysics and Biomolecular Structure, 36, 191, 10.1146/annurev.biophys.35.040405.102002 Bhattacharya, 2011, A deterministic map of Waddington's epigenetic landscape for cell fate specification, BMC Systems Biology, 5, 85, 10.1186/1752-0509-5-85 Bolouri, 2008 Cai, 2020, Enhancer dependence of cell-type-specific gene expression increases with developmental age, Proceedings of the National Academy of Sciences of the United States of America, 117, 21450, 10.1073/pnas.2008672117 Cameron, 2006, Unusual gene order and organization of the sea urchin hox cluster, Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 306, 45, 10.1002/jez.b.21070 Carroll, 2013 Carroll, 1995, Homeotic genes and the regulation and evolution of insect wing number, Nature, 375, 58, 10.1038/375058a0 Cary, 2017, Genome-wide use of high- and low-affinity Tbrain transcription factor binding sites during echinoderm development, Proceedings of the National Academy of Sciences of the United States of America, 114, 5854, 10.1073/pnas.1610611114 Cary, 2020 Cheatle Jarvela, 2014, Modular evolution of DNA-binding preference of a Tbrain transcription factor provides a mechanism for modifying gene regulatory networks, Molecular Biology and Evolution, 31, 2672, 10.1093/molbev/msu213 Christiaen, 2008, The transcription/migration interface in heart precursors of Ciona intestinalis, Science, 320, 1349, 10.1126/science.1158170 Conant, 2003, Convergent evolution of gene circuits, Nature Genetics, 34, 264, 10.1038/ng1181 Crocker, 2016, The soft touch: Low-affinity transcription factor binding sites in development and evolution, Current Topics in Developmental Biology, 117, 455, 10.1016/bs.ctdb.2015.11.018 Darbellay, 2019, The constrained architecture of mammalian Hox gene clusters, Proceedings of the National Academy of Sciences of the United States of America, 116, 13424, 10.1073/pnas.1904602116 Davidson, 2010, Emerging properties of animal gene regulatory networks, Nature, 468, 911, 10.1038/nature09645 Davidson, 2006, Gene regulatory networks and the evolution of animal body plans, Science, 311, 796, 10.1126/science.1113832 Davidson, 2009, An integrated view of precambrian eumetazoan evolution, Cold Spring Harbor Symposia on Quantitative Biology, 74, 65, 10.1101/sqb.2009.74.042 Deschamps, 2005, Developmental regulation of the Hox genes during axial morphogenesis in the mouse, Development, 132, 2931, 10.1242/dev.01897 Ding, 2020, Analysis of time series regulatory networks, Current Opinion in Systems Biology, 21, 16, 10.1016/j.coisb.2020.07.005 Domazet-Lošo, 2010, A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns, Nature, 468, 815, 10.1038/nature09632 Drapek, 2017, Uncovering gene regulatory networks controlling plant cell differentiation, Trends in Genetics, 33, 529, 10.1016/j.tig.2017.05.002 Erwin, 2009, The evolution of hierarchical gene regulatory networks, Nature Reviews. Genetics, 10, 141, 10.1038/nrg2499 Ettensohn, 1993, Mesodermal cell interactions in the sea urchin embryo: properties of skeletogenic secondary mesenchyme cells, Development, 117, 1275, 10.1242/dev.117.4.1275 Flower, 2020, How to visualize cells as overlapping trajectories of profiles, 356 Force, 1999, Preservation of duplicate genes by complementary, degenerative mutations, Genetics, 151, 1531, 10.1093/genetics/151.4.1531 Franchini, 2011, Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons, Proceedings of the National Academy of Sciences of the United States of America, 108, 15270, 10.1073/pnas.1104997108 Frankel, 2012, Conserved regulatory architecture underlies parallel genetic changes and convergent phenotypic evolution, Proceedings of the National Academy of Sciences of the United States of America, 109, 20975, 10.1073/pnas.1207715109 Freckelton, 2017, Induction of invertebrate larval settlement; different bacteria, different mechanisms?, Scientific Reports, 7, 42557, 10.1038/srep42557 Friedman, 2018, Single-cell transcriptomic analysis of cardiac differentiation from human PSCs reveals HOPX-dependent cardiomyocyte maturation, Cell Stem Cell, 23, 586, 10.1016/j.stem.2018.09.009 Furuta, 2018, Laminin signals initiate the reciprocal loop that informs breast-specific gene expression and homeostasis by activating NO, p53 and microRNAs, elife, 7, 10.7554/eLife.26148 Gao, 2008, Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution, Proceedings of the National Academy of Sciences of the United States of America, 105, 6091, 10.1073/pnas.0801201105 Garcia-Fernàndez, 2005, Hox, ParaHox, ProtoHox: Facts and guesses, Heredity, 94, 145, 10.1038/sj.hdy.6800621 Gehrke, 2019, Acoel genome reveals the regulatory landscape of whole-body regeneration, Science, 363, eaau6173, 10.1126/science.aau6173 Gilbert, 2000 Gilbert, 2003, Evo-devo, devo-evo, and devgen-popgen, Biology and Philosophy, 18, 347, 10.1023/A:1023944304419 Gilbert, 1996, Resynthesizing evolutionary and developmental biology, Developmental Biology, 173, 357, 10.1006/dbio.1996.0032 Gillis, 2012, A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network, Proceedings. Biological Sciences/the Royal Society, 279, 237, 10.1098/rspb.2011.0599 Graf, 2009, Forcing cells to change lineages, Nature, 462, 587, 10.1038/nature08533 Graham, 2012, Developmental and evolutionary origins of the pharyngeal apparatus, EvoDevo, 3, 24, 10.1186/2041-9139-3-24 Hall, 2003, Unlocking the black box between genotype and phenotype: Cell condensations as morphogenetic (modular) units, Biology and Philosophy, 18, 219, 10.1023/A:1023984018531 Hamouda, 2020, Nuclear mechanotransduction in stem cells, Current Opinion in Cell Biology, 64, 97, 10.1016/j.ceb.2020.05.005 Han, 2004, Evidence for dynamically organized modularity in the yeast protein-protein interaction network, Nature, 430, 88, 10.1038/nature02555 He, 2010, Hierarchical evolution of animal body plans, Developmental Biology, 337, 157, 10.1016/j.ydbio.2009.09.038 He, 2011, Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules, PLoS Genetics, 7, 10.1371/journal.pgen.1002053 Hill, 2017, Heart morphogenesis gene regulatory networks revealed by temporal expression analysis, Development, 144, 3487 Hinman, 2003, Developmental gene regulatory network architecture across 500 million years of echinoderm evolution, Proceedings of the National Academy of Sciences of the United States of America, 100, 13356, 10.1073/pnas.2235868100 Holland, 1996, Expression of AmphiHox-1 and AmphiPax-1 in amphioxus embryos treated with retinoic acid: Insights into evolution and patterning of the chordate nerve cord and pharynx, Development, 122, 1829, 10.1242/dev.122.6.1829 Hong, 2008, Shadow enhancers as a source of evolutionary novelty, Science, 321, 1314, 10.1126/science.1160631 Illmensee, 1976, Totipotency and normal differentiation of single teratocarcinoma cells cloned by injection into blastocysts, Proceedings of the National Academy of Sciences of the United States of America, 73, 549, 10.1073/pnas.73.2.549 Israel, 2016, Comparative developmental transcriptomics reveals rewiring of a highly conserved gene regulatory network during a major life history switch in the sea urchin genus heliocidaris, PLoS Biology, 14, 10.1371/journal.pbio.1002391 Kasemeier-Kulesa, 2008, Reprogramming multipotent tumor cells with the embryonic neural crest microenvironment, Developmental Dynamics, 237, 2657, 10.1002/dvdy.21613 Keller, 2002 Kenny, 2003, Tumor reversion: Correction of malignant behavior by microenvironmental cues, International Journal of Cancer, 107, 688, 10.1002/ijc.11491 Khalturin, 2020, The origin of metazoan larvae, Nature Ecology & Evolution, 4, 674, 10.1038/s41559-020-1192-8 Kirchhamer, 1996, Modular cis-regulatory organization of developmentally expressed genes: Two genes transcribed territorially in the sea urchin embryo, and additional examples, Proceedings of the National Academy of Sciences of the United States of America, 93, 9322, 10.1073/pnas.93.18.9322 Klingenberg, 1996, Multivariate allometry, 23 Kmita, 2002, Serial deletions and duplications suggest a mechanism for the collinearity of Hoxd genes in limbs, Nature, 420, 145, 10.1038/nature01189 Kozmik, 2007, Pax-Six-Eya-Dach network during amphioxus development: Conservation in vitro but context specificity in vivo, Developmental Biology, 306, 143, 10.1016/j.ydbio.2007.03.009 Krause, 2003, Compartments revealed in food-web structure, Nature, 426, 282, 10.1038/nature02115 Ladewig, 2013, Leveling Waddington: The emergence of direct programming and the loss of cell fate hierarchies, Nature Reviews. Molecular Cell Biology, 14, 225, 10.1038/nrm3543 Levin, 2016, The mid-developmental transition and the evolution of animal body plans, Nature, 531, 637, 10.1038/nature16994 Levine, 2005, Gene regulatory networks for development, Proceedings of the National Academy of Sciences of the United States of America, 102, 4936, 10.1073/pnas.0408031102 Lonfat, 2014, Convergent evolution of complex regulatory landscapes and pleiotropy at Hox loci, Science, 346, 1004, 10.1126/science.1257493 Longabaugh, 2005, Computational representation of developmental genetic regulatory networks, Developmental Biology, 283, 1, 10.1016/j.ydbio.2005.04.023 Ludwig, 1995, Evolutionary dynamics of the enhancer region of even-skipped in Drosophila, Molecular Biology and Evolution, 12, 1002 Lynch, 2015, Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy, Cell Reports, 10, 551, 10.1016/j.celrep.2014.12.052 Maeso, 2013, Deep conservation of cis-regulatory elements in metazoans, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 368 Marlow, 2014, Larval body patterning and apical organs are conserved in animal evolution, BMC Biology, 12, 7, 10.1186/1741-7007-12-7 Martik, 2015, Deployment of a retinal determination gene network drives directed cell migration in the sea urchin embryo, eLife, 4, e08827, 10.7554/eLife.08827 McCauley, 2010, A conserved gene regulatory network subcircuit drives different developmental fates in the vegetal pole of highly divergent echinoderm embryos, Developmental Biology, 340, 200, 10.1016/j.ydbio.2009.11.020 McEwen, 2009, Early evolution of conserved regulatory sequences associated with development in vertebrates, PLoS Genetics, 5, 10.1371/journal.pgen.1000762 McQueen, 2020, On the specificity of gene regulatory networks: How does network co-option affect subsequent evolution?, Current Topics in Developmental Biology, 139, 375, 10.1016/bs.ctdb.2020.03.002 Melo, 2016, Modularity: Genes, development and evolution, Annual Review of Ecology, Evolution, and Systematics, 47, 463, 10.1146/annurev-ecolsys-121415-032409 Mitteroecker, 2009, The developmental basis of variational modularity: Insights from quantitative genetics, morphometrics, and developmental biology, Evolutionary Biology, 36, 377, 10.1007/s11692-009-9075-6 Moignard, 2015, Decoding the regulatory network of early blood development from single-cell gene expression measurements, Nature Biotechnology, 33, 269, 10.1038/nbt.3154 Monteiro, 2008, Alternative models for the evolution of eyespots and of serial homology on lepidopteran wings, BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 30, 358, 10.1002/bies.20733 Monteiro, 2016, Identifying coopted networks and causative mutations in the origin of novel complex traits, Current Topics in Developmental Biology, 119, 205, 10.1016/bs.ctdb.2016.03.003 Monteiro, 2009, Wings, horns, and butterfly eyespots: How do complex traits evolve?, PLoS Biology, 7, 10.1371/journal.pbio.1000037 Nakagawa, 2013, DNA-binding specificity changes in the evolution of forkhead transcription factors, Proceedings of the National Academy of Sciences of the United States of America, 110, 12349, 10.1073/pnas.1310430110 Navratilova, 2009, Systematic human/zebrafish comparative identification of cis-regulatory activity around vertebrate developmental transcription factor genes, Developmental Biology, 327, 526, 10.1016/j.ydbio.2008.10.044 Nelson, 2013, Conserved non-coding elements and cis regulation: Actions speak louder than words, Development, 140, 1385, 10.1242/dev.084459 Novershtern, 2011, Densely interconnected transcriptional circuits control cell states in human hematopoiesis, Cell, 144, 296, 10.1016/j.cell.2011.01.004 Ochoterena, 2019, The search for common origin: Homology revisited, Systematic Biology, 68, 767, 10.1093/sysbio/syz013 Ogasawara, 1999, Developmental expression of Pax1/9 genes in urochordate and hemichordate gills: Insight into function and evolution of the pharyngeal epithelium, Development, 126, 2539, 10.1242/dev.126.11.2539 Oliveri, 2002, A regulatory gene network that directs micromere specification in the sea urchin embryo, Developmental Biology, 246, 209, 10.1006/dbio.2002.0627 Oliveri, 2004, Gene regulatory network controlling embryonic specification in the sea urchin, Current Opinion in Genetics & Development, 14, 351, 10.1016/j.gde.2004.06.004 Oliveri, 2008, Global regulatory logic for specification of an embryonic cell lineage, Proceedings of the National Academy of Sciences of the United States of America, 105, 5955, 10.1073/pnas.0711220105 Olson, 2006, Gene regulatory networks in the evolution and development of the heart, Science, 313, 1922, 10.1126/science.1132292 Partha, 2017, Subterranean mammals show convergent regression in ocular genes and enhancers, along with adaptation to tunneling, eLife, 6, e25884, 10.7554/eLife.25884 Peter, 2009, Modularity and design principles in the sea urchin embryo gene regulatory network, FEBS Letters, 583, 3948, 10.1016/j.febslet.2009.11.060 Piccus, 2020, The nuclear envelope: LINCing tissue mechanics to genome regulation in cardiac and skeletal muscle, Biology Letters, 16, 10.1098/rsbl.2020.0302 Preger-Ben Noon, 2018, Comprehensive analysis of a cis-regulatory region reveals pleiotropy in enhancer function, Cell Reports, 22, 3021, 10.1016/j.celrep.2018.02.073 Qin, 2020, Molecular mechanosensors in osteocytes, Bone Research, 8 Raff, 1996 Raff, 1991 Rafiq, 2012, The genomic regulatory control of skeletal morphogenesis in the sea urchin, Development, 139, 579, 10.1242/dev.073049 Ramos, 2013, Low-affinity transcription factor binding sites shape morphogen responses and enhancer evolution, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 368, 20130018, 10.1098/rstb.2013.0018 Ravasz, 2002, Hierarchical organization of modularity in metabolic networks, Science, 297, 1551, 10.1126/science.1073374 Reiter, 2017, Combinatorial function of transcription factors and cofactors, Current Opinion in Genetics & Development, 43, 73, 10.1016/j.gde.2016.12.007 Relaix, 1999, From insect eye to vertebrate muscle: Redeployment of a regulatory network, Genes & Development, 13, 3171, 10.1101/gad.13.24.3171 Ritschar, 2020, Predator-specific inducible morphological defenses of a water flea against two freshwater predators, Journal of Morphology, 281, 653, 10.1002/jmor.21131 Ritter, 2010, The importance of being cis: Evolution of orthologous fish and mammalian enhancer activity, Molecular Biology and Evolution, 27, 2322, 10.1093/molbev/msq128 Rozowski, 2002, Hox gene control of segment-specific bristle patterns in Drosophila, Genes & Development, 16, 1150, 10.1101/gad.219302 Sabarís, 2019, Actors with multiple roles: Pleiotropic enhancers and the paradigm of enhancer modularity, Trends in Genetics, 35, 423, 10.1016/j.tig.2019.03.006 Sandve, 2018, Subfunctionalization versus neofunctionalization after whole-genome duplication, Nature Genetics, 50, 908, 10.1038/s41588-018-0162-4 Sareen, 2010, Stem cell biologists sure play a mean pinball, Nature Biotechnology, 28, 333, 10.1038/nbt0410-333 Sayed, 2018, Automated extension of cell signaling models with genetic algorithm, Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 2018, 5030 Segal, 2008, Predicting expression patterns from regulatory sequence in Drosophila segmentation, Nature, 451, 535, 10.1038/nature06496 Shubin, 2009, Deep homology and the origins of evolutionary novelty, Nature, 457, 818, 10.1038/nature07891 Siegal, 2002, Waddington's canalization revisited: Developmental stability and evolution, Proceedings of the National Academy of Sciences of the United States of America, 99, 10528, 10.1073/pnas.102303999 Simakov, 2015, Hemichordate genomes and deuterostome origins, Nature, 527, 459, 10.1038/nature16150 Simon, 1962, The architecture of complexity, Proceedings of the American Philosophical Society, 106, 467 Smith, 2011, Regeneration in the era of functional genomics and gene network analysis, The Biological Bulletin, 221, 18, 10.1086/BBLv221n1p18 Smith, 2007, A gene regulatory network subcircuit drives a dynamic pattern of gene expression, Science, 318, 794, 10.1126/science.1146524 Stern, 2000, Evolutionary developmental biology and the problem of variation, Evolution, 54, 1079 Takahashi, 2012, Cellular reprogramming—lowering gravity on Waddington's epigenetic landscape, Journal of Cell Science, 125, 2553 Tran, 2011, Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria, Marine Ecology Progress Series, 433, 85, 10.3354/meps09192 Tuğrul, 2015, Dynamics of transcription factor binding site evolution, PLoS Genetics, 11, 10.1371/journal.pgen.1005639 von Baer, 1828 Waddington, 1957 Wagner, 2007, The developmental genetics of homology, Nature Reviews. Genetics, 8, 473, 10.1038/nrg2099 Wagner, 2007, The road to modularity, Nature Reviews. Genetics, 8, 921, 10.1038/nrg2267 Wagner, 2018, Single-cell mapping of gene expression landscapes and lineage in the zebrafish embryo, Science, 360, 981, 10.1126/science.aar4362 Wang, 2020, Evolutionary transcriptomics of metazoan biphasic life cycle supports a single intercalation origin of metazoan larvae, Nature Ecology & Evolution, 4, 725, 10.1038/s41559-020-1138-1 West-Eberhard, 2019, Modularity as a universal emergent property of biological traits, Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 332, 356, 10.1002/jez.b.22913 Wittkopp, 2011, Cis-regulatory elements: Molecular mechanisms and evolutionary processes underlying divergence, Nature Reviews. Genetics, 13, 59, 10.1038/nrg3095 Wu, 2013, Hierarchy theory: An overview, 281 Xue, 2013, Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing, Nature, 500, 593, 10.1038/nature12364 Yáñez-Cuna, 2012, Uncovering cis-regulatory sequence requirements for context-specific transcription factor binding, Genome Research, 22, 2018, 10.1101/gr.132811.111 Yin, 2017, Hidden defensive morphology in rotifers: Benefits, costs, and fitness consequences, Scientific Reports, 7, 4488, 10.1038/s41598-017-04809-z Zhu, 2012, Differential regulation of mesodermal gene expression by Drosophila cell type-specific Forkhead transcription factors, Development, 139, 1457, 10.1242/dev.069005