Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements
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Bilaterian animals have a Hox gene cluster essential for patterning the main body axis, and a ParaHox gene cluster. Comparison of Hox and ParaHox genes has led workers to postulate that both clusters originated from the duplication of an ancient cluster named ProtoHox, which contained up to four genes with at least the precursors of anterior and posterior Hox/ParaHox genes. However, the way in which genes diversified within the ProtoHox, Hox and ParaHox clusters remains unclear because no systematic study of non-bilaterian animals exists. Here we characterize the full Hox/ParaHox gene complements and genomic organization in two cnidarian species (Nematostella vectensis and Hydra magnipapillata), and suggest a ProtoHox cluster simpler than originally thought on the basis of three arguments. First, both species possess bilaterian-like anterior Hox genes, but their non-anterior genes do not appear as counterparts of either bilaterian central or posterior genes; second, two clustered ParaHox genes, Gsx and a gene related to Xlox and Cdx, are found in Nematostella vectensis; and third, we do not find clear phylogenetic support for a common origin of bilaterian Cdx and posterior genes, which might therefore have appeared after the ProtoHox cluster duplication. Consequently, the ProtoHox cluster might have consisted of only two anterior genes. Non-anterior genes could have appeared independently in the Hox and ParaHox clusters, possibly after the separation of bilaterians and cnidarians.
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Seven putative ancestral eumetazoan linkage groups link anemone scaffolds to multiple regions of the human genome in a manner consistent with multiple large-scale duplication events along the vertebrate lineage.
“Seven of the PALs link anemone scaffolds to multiple regions of the human genome in a manner consistent with multiple large-scale duplication events along the vertebrate lineage (reviewed, for example, in (53)).”
From Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization (2007) · cites this paper as [53]
Cites
Homeobox genes and axial patterning
McGinnis, W., & Krumlauf, R. (1992) · Cell · doi:10.1016/0092-8674(92)90471-n · Cited by 2,674 · see citing works
Philippe, H., Lartillot, N., & Brinkmann, H. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi111 · Cited by 551 · see citing works
The genesis and evolution of homeobox gene clusters
García‐Fernàndez, J. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1723 · Cited by 478 · see citing works
The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster
Brooke, N. M., Garcia-Fernàndez, J., & Holland, P. W. H. (1998) · Nature · doi:10.1038/31933 · Cited by 468 · see citing works
Origins of Bilateral Symmetry: <i>Hox</i> and <i>Dpp</i> Expression in a Sea Anemone
Finnerty, J. R., Pang, K., Burton, P., Paulson, D., & Martindale, M. Q. (2004) · Science · doi:10.1126/science.1091946 · Cited by 407 · see citing works
Phylogeny of Medusozoa and the evolution of cnidarian life cycles
Collins, A. G. (2002) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.2002.00403.x · Cited by 355 · see citing works
Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians
Technau, U., Rudd, S., Maxwell, P., Gordon, P. M. K., Saina, M., Grasso, L. C., Hayward, D. C., Sensen, C. W., Saint, R., Holstein, T. W., et al. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.09.007 · Cited by 337 · see citing works
Self-citationAncient origin of the Hox gene cluster
Ferrier, D. E. K., & Holland, P. W. H. (2001) · Nature Reviews Genetics · doi:10.1038/35047605 · Cited by 260 · see citing works
Collins, A. G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15458 · Cited by 252 · see citing works
Rising starlet: the starlet sea anemone,Nematostella vectensis
Darling, J. A., Reitzel, A. M., Burton, P. M., Mazza, M. E., Ryan, J. F., Sullivan, J. C., & Finnerty, J. R. (2005) · BioEssays · doi:10.1002/bies.20181 · Cited by 214 · see citing works
Gauchat, D., Mazet, F., Berney, C., Schummer, M., Kreger, S., Pawlowski, J., & Galliot, B. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4493 · Cited by 190 · see citing works
Evolution of striated muscle: Jellyfish and the origin of triploblasty
Seipel, K., & Schmid, V. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.03.032 · Cited by 172 · see citing works
Ancient origins of axial patterning genes: Hox genes and ParaHox genes in the Cnidaria
Finnerty, J. R., & Martindale, M. Q. (1999) · Evolution & Development · doi:10.1046/j.1525-142x.1999.99010.x · Cited by 152 · see citing works
Shenk, M. A., Bode, H. R., & Steele, R. E. (1993) · Development · doi:10.1242/dev.117.2.657 · Cited by 129 · see citing works
Self-citationEarly evolution of a homeobox gene: the parahox gene Gsx in the Cnidaria and the Bilateria
Finnerty, J. R., Paulson, D. A., Burton, P. M., Pang, K., & Martindale, M. Q. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03041.x · Cited by 85 · see citing works
Homeobox genes and the zootype
Miller, D. J., & Miles, A. (1993) · Nature · doi:10.1038/365215b0 · Cited by 74 · see citing works
Cnidarian homeoboxes and the zootype
Martínez, D. E., Bridge, D., Masuda-Nakagawa, L. M., & Cartwright, P. (1998) · Nature · doi:10.1038/31616 · Cited by 66 · see citing works
A low diversity of ANTP class homeobox genes in Placozoa
Monteiro, A. S., Schierwater, B., Dellaporta, S. L., & Holland, P. W. H. (2006) · Evolution & Development · doi:10.1111/j.1525-142x.2006.00087.x · Cited by 61 · see citing works
Kuhn, K., Streit, B., & Schierwater, B. (1996) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.1996.0055 · Cited by 58 · see citing works
Chromosomal mapping of ANTP class homeobox genes in amphioxus: piecing together ancestral genomes
Castro, L. F. C., & Holland, P. W. H. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03052.x · Cited by 55 · see citing works
Snell, E. A., Scemama, J., & Stellwag, E. J. (1999) · Journal of Experimental Zoology · doi:10.1002/(sici)1097-010x(19990415)285:1 · Cited by 25 · see citing works
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Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization
Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., et al. (2007) · Science · doi:10.1126/science.1139158 · Cited by 1,555 · see citing works
Self-citationGenome Regulation by Polycomb and Trithorax Proteins
Schuettengruber, B., Chourrout, D. M., Vervoort, M., Leblanc, B., & Cavalli, G. (2007) · Cell · doi:10.1016/j.cell.2007.02.009 · Cited by 1,433 · see citing works
Self-citationChapman, J. A., Kirkness, E. F., Simakov, O., Hampson, S. E., Mitros, T., Weinmaier, T., Rattei, T., Balasubramanian, P. G., Borman, J., Busam, D., et al. (2010) · Nature · doi:10.1038/nature08830 · Cited by 810 · see citing works
Self-citationSchnittger, L., Rodríguez, A. E., Florin‐Christensen, M., & Morrison, D. A. (2012) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2012.07.004 · Cited by 601 · see citing works
The rise and fall of Hox gene clusters
Duboule, D. (2007) · Development · doi:10.1242/dev.001065 · Cited by 525 · see citing works
The deep evolution of metazoan microRNAs
Wheeler, B. M., Heimberg, A. M., Moy, V. N., Sperling, E. A., Holstein, T. W., Heber, S., & Peterson, K. J. (2009) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00302.x · Cited by 473 · see citing works
The genome of Aiptasia , a sea anemone model for coral symbiosis
Baumgarten, S., Simakov, O., Esherick, L. Y., Liew, Y. J., Lehnert, E. M., Michell, C., Li, Y., Hambleton, E. A., Guse, A., Oates, M. E., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1513318112 · Cited by 438 · see citing works
Homeodomain proteins: an update
Bürglin, T. R., & Affolter, M. (2015) · Chromosoma · doi:10.1007/s00412-015-0543-8 · Cited by 435 · see citing works
The innate immune repertoire in Cnidaria - ancestral complexity and stochastic gene loss
Miller, D. J., Hemmrich, G., Ball, E. E., Hayward, D. C., Khalturin, K., Funayama, N., Agata, K., & Bosch, T. C. G. (2007) · Genome biology · doi:10.1186/gb-2007-8-4-r59 · Cited by 390 · see citing works
Six major steps in animal evolution: Are we derived sponge larvae?
Nielsen, C. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00231.x · Cited by 343 · see citing works
Holland, P. W. H. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.78 · Cited by 312 · see citing works
From nerve net to nerve ring, nerve cord and brain — evolution of the nervous system
Arendt, D., Tosches, M. A., & Marlow, H. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.15 · Cited by 279 · see citing works
Simionato, E., Ledent, V., Richards, G. S., Thomas‐Chollier, M., Kerner, P., Coornaert, D., Degnan, B. M., & Vervoort, M. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-33 · Cited by 289 · see citing works
Genesis and Expansion of Metazoan Transcription Factor Gene Classes
Larroux, C., Luke, G. N., Koopman, P. A., Rokhsar, D. S., Shimeld, S. M., & Degnan, B. M. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn047 · Cited by 275 · see citing works
Evolutionary crossroads in developmental biology: Cnidaria
Technau, U., & Steele, R. E. (2011) · Development · doi:10.1242/dev.048959 · Cited by 274 · see citing works
Self-citationCdx and Hox Genes Differentially Regulate Posterior Axial Growth in Mammalian Embryos
Young, T., Rowland, J., van de Ven, C., Bialecka, M., Nóvoa, A., Carapuço, M., van Nes, J., de Graaff, W., Duluc, I., Freund, J., et al. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.08.010 · Cited by 258 · see citing works
Ryan, J. F., Mazza, M. E., Pang, K., Matus, D. Q., Baxevanis, A. D., Martindale, M. Q., & Finnerty, J. R. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000153 · Cited by 241 · see citing works
Evolution of genome architecture
Koonin, E. V. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.09.015 · Cited by 215 · see citing works
Osbourn, A., & Field, B. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0114-3 · Cited by 213 · see citing works
Cnidarians and the evolutionary origin of the nervous system
Watanabe, H., Fujisawa, T., & Holstein, T. W. (2009) · Development, Growth & Differentiation · doi:10.1111/j.1440-169x.2009.01103.x · Cited by 206 · see citing works
MicroRNAs in the Hox network: an apparent link to posterior prevalence
Yekta, S., Tabin, C. J., & Bartel, D. P. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2400 · Cited by 198 · see citing works
The chromatin insulator CTCF and the emergence of metazoan diversity
Heger, P., Marin, B., Bartkuhn, M., Schierenberg, E., & Wiehe, T. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111941109 · Cited by 193 · see citing works
Evolutionary conservation of the eumetazoan gene regulatory landscapePreprint
Schwaiger, M., Schönauer, A., Rendeiro, A. F., Pribitzer, C., Schauer, A., Gilles, A. F., Schinko, J. B., Renfer, E., Fredman, D., & Technau, U. (2014) · Genome Research · doi:10.1101/gr.162529.113 · Cited by 188 · see citing works
Self-citationThe genome of the jellyfish Clytia hemisphaerica and the evolution of the cnidarian life-cycle
Leclère, L., Horin, C., Chevalier, S., Lapébie, P., Dru, P., Péron, S., Jager, M., Condamine, T., Pottin, K., Romano, S., et al. (2019) · Nature Ecology & Evolution · doi:10.1038/s41559-019-0833-2 · Cited by 190 · see citing works
Self-citationThe Wnt code: cnidarians signal the way
Guder, C., Philipp, I., Lengfeld, T., Watanabe, H., Hobmayer, B., & Holstein, T. W. (2006) · Oncogene · doi:10.1038/sj.onc.1210052 · Cited by 177 · see citing works
The NK homeobox gene cluster predates the origin of Hox genes.
Larroux, C., Fahey, B., Degnan, S. M., Adamski, M., Rokhsar, D. S., & Degnan, B. M. (2007) · Current Biology · doi:10.1016/j.cub.2007.03.008 · Cited by 173 · see citing works
Origins of neurogenesis, a cnidarian view
Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M., & Chera, S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.563 · Cited by 168 · see citing works
FGF signalling controls formation of the apical sensory organ in the cnidarianNematostella vectensis
Rentzsch, F., Fritzenwanker, J. H., Scholz, C. B., & Technau, U. (2008) · Development · doi:10.1242/dev.020784 · Cited by 166 · see citing works
Self-citationRentzsch, F., Anton, R., Saina, M., Hammerschmidt, M., Holstein, T. W., & Technau, U. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.06.003 · Cited by 170 · see citing works
Self-citationAcoel development supports a simple planula-like urbilaterian
Hejnol, A., & Martindale, M. Q. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2239 · Cited by 161 · see citing works
Ryan, J. F., Pang, K., Program, N. C. S., Mullikin, J. C., Martindale, M. Q., & Baxevanis, A. D. (2010) · EvoDevo · doi:10.1186/2041-9139-1-9 · Cited by 160 · see citing works
An axial Hox code controls tissue segmentation and body patterning in Nematostella vectensis
He, S., Viso, F. D., Chen, C., Ikmi, A., Kroesen, A. E., & Gibson, M. C. (2018) · Science · doi:10.1126/science.aar8384 · Cited by 148 · see citing works
Medusozoan genomes inform the evolution of the jellyfish body plan
Khalturin, K., Shinzato, C., Khalturina, M., Hamada, M., Fujie, M., Koyanagi, R., Kanda, M., Goto, H., Anton‐Erxleben, F., Toyokawa, M., et al. (2019) · Nature Ecology & Evolution · doi:10.1038/s41559-019-0853-y · Cited by 135 · see citing works
The genome of the jellyfish Aurelia and the evolution of animal complexity
Gold, D. A., Katsuki, T., Li, Y., Yan, X., Regulski, M., Ibberson, D., Holstein, T. W., Steele, R. E., Jacobs, D. K., & Greenspan, R. J. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0719-8 · Cited by 142 · see citing works
Self-citationEarly development and axis specification in the sea anemone Nematostella vectensis
Fritzenwanker, J. H., Genikhovich, G., Kraus, Y. A., & Technau, U. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.07.029 · Cited by 140 · see citing works
Self-citationMukherjee, K., & Bürglin, T. R. (2007) · Journal of Molecular Evolution · doi:10.1007/s00239-006-0023-0 · Cited by 141 · see citing works
Early evolution of metazoan transcription factors
Degnan, B. M., Vervoort, M., Larroux, C., & Richards, G. S. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.09.008 · Cited by 137 · see citing works
Evolution of the Insect Yellow Gene Family
Ferguson, L. C., Green, J. E., Surridge, A. K., & Jiggins, C. D. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq192 · Cited by 128 · see citing works
On the evolution of bilaterality
Genikhovich, G., & Technau, U. (2017) · Development · doi:10.1242/dev.141507 · Cited by 121 · see citing works
Self-citationHox genes in development and beyond
Hubert, K. A., & Wellik, D. M. (2023) · Development · doi:10.1242/dev.192476 · Cited by 120 · see citing works
Early evolution of symmetry and polarity in metazoan body plans
Manuel, M. (2008) · Comptes Rendus Biologies · doi:10.1016/j.crvi.2008.07.009 · Cited by 123 · see citing works
Topological structures and syntenic conservation in sea anemone genomes
Zimmermann, B., Montenegro, J. D., Robb, S. M. C., Fropf, W. J., Weilguny, L., He, S., Chen, S., Lovegrove-Walsh, J., Hill, E. M., Chen, C.-Y., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-44080-7 · Cited by 106 · see citing works
Self-citationCnidarian microRNAs frequently regulate targets by cleavagePreprint
Moran, Y., Fredman, D., Praher, D., Li, X. Z., Wee, L. M., Rentzsch, F., Zamore, P. D., Technau, U., & Seitz, H. (2014) · Genome Research · doi:10.1101/gr.162503.113 · Cited by 109 · see citing works
Self-citationA genomic view of 500 million years of cnidarian evolution
Steele, R. E., David, C. N., & Technau, U. (2011) · Trends in Genetics · doi:10.1016/j.tig.2010.10.002 · Cited by 111 · see citing works
Self-citationBack in time: a new systematic proposal for the Bilateria
Baguñà, J., Martinez, P., Paps, J., & Riutort, M. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2238 · Cited by 105 · see citing works
Rethinking the role of immunity: lessons from Hydra
Bosch, T. C. G. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.07.008 · Cited by 105 · see citing works
Calcisponges have a ParaHox gene and dynamic expression of dispersed NK homeobox genes
Fortunato, S., Adamski, M., Ramos, O. M., Leininger, S., Liu, J. L., Ferrier, D. E. K., & Adamska, M. (2014) · Nature · doi:10.1038/nature13881 · Cited by 104 · see citing works
Evolution of Networks for Body Plan Patterning; Interplay of Modularity, Robustness and Evolvability
ten Tusscher, K., & Hogeweg, P. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002208 · Cited by 101 · see citing works
Chiori, R., Jager, M., Denker, E., Wincker, P., Silva, C. D., Guyader, H. L., Manuel, M., & Quéinnec, É. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004231 · Cited by 97 · see citing works
Ereskovsky, A. V., Borchiellini, C., Gazave, E., Ivanišević, J., Lapébie, P., Pérez, T., Renard, E., & Vacelet, J. (2009) · BioEssays · doi:10.1002/bies.080058 · Cited by 93 · see citing works
Segmentation, metamerism and the Cambrian explosion
Couso, J. P. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.072425jc · Cited by 95 · see citing works
Embryonic development and metamorphosis of the scyphozoan Aurelia
Yuan, D., Nakanishi, N., Jacobs, D. K., & Hartenstein, V. (2008) · Development Genes and Evolution · doi:10.1007/s00427-008-0254-8 · Cited by 83 · see citing works
Cartwright, P., & Collins, A. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm071 · Cited by 57 · see citing works
Ying, H., Cooke, I., Sprungala, S., Wang, W., Hayward, D. C., Tang, Y., Huttley, G. A., Ball, E. E., Forêt, S., & Miller, D. J. (2018) · Genome biology · doi:10.1186/s13059-018-1552-8 · Cited by 82 · see citing works
An ancient chordin-like gene in organizer formation of Hydra
Rentzsch, F., Guder, C., Vocke, D., Hobmayer, B., & Holstein, T. W. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604501104 · Cited by 81 · see citing works
Self-citationHejnol, A., & Martindale, M. Q. (2009) · BMC Biology · doi:10.1186/1741-7007-7-65 · Cited by 80 · see citing works
Ohdera, A. H., Ames, C. L., Dikow, R. B., Kayal, E., Chiodin, M., Busby, B., La, S., Pirro, S., Collins, A. G., Medina, M., et al. (2019) · GigaScience · doi:10.1093/gigascience/giz069 · Cited by 77 · see citing works
Onai, T., Lin, H., Schubert, M., Koop, D., Osborne, P. W., Álvarez, S., Álvarez, R., Holland, N. D., & Holland, L. Z. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.571 · Cited by 75 · see citing works
Duplicated Hox genes in the spider Cupiennius salei
Schwager, E. E., Schoppmeier, M., Pechmann, M., & Damen, W. G. M. (2007) · Frontiers in Zoology · doi:10.1186/1742-9994-4-10 · Cited by 75 · see citing works
Gómez, C. M. A., Sabin, K., & Echeverri, K. (2020) · Developmental Dynamics · doi:10.1002/dvdy.178 · Cited by 66 · see citing works
Hox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation
DuBuc, T. Q., Stephenson, T. B., Rock, A. Q., & Martindale, M. Q. (2018) · Nature Communications · doi:10.1038/s41467-018-04184-x · Cited by 73 · see citing works
The genetic factors of bilaterian evolution
Heger, P., Zheng, W. L., Rottmann, A., Panfilio, K. A., & Wiehe, T. (2020) · eLife · doi:10.7554/elife.45530 · Cited by 75 · see citing works
Evolutionary crossroads in developmental biology
Patel, N. H. (2012) · Development · doi:10.1242/dev.085464 · Cited by 74 · see citing works
Niwa, H., Sekita, Y., Tsend‐Ayush, E., & Grützner, F. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00280.x · Cited by 68 · see citing works
Burton, P. M., & Finnerty, J. R. (2009) · Development Genes and Evolution · doi:10.1007/s00427-009-0271-2 · Cited by 66 · see citing works
Ancestral and recently recruited global control of the Hox genes in development
Deschamps, J. (2007) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2007.07.008 · Cited by 65 · see citing works
The genome of the giant Nomura’s jellyfish sheds light on the early evolution of active predation
Kim, H., Weber, J. A., Lee, N., Park, S. G., Cho, Y. S., Bhak, Y., Lee, N., Jeon, Y., Jeon, S., Luria, V. A., et al. (2019) · BMC Biology · doi:10.1186/s12915-019-0643-7 · Cited by 63 · see citing works
MAPK signaling is necessary for neurogenesis in Nematostella vectensis
Layden, M. J., Johnston, H. T., Amiel, A., Havrilak, J. A., Steinworth, B. M., Chock, T., Röttinger, É., & Martindale, M. Q. (2016) · BMC Biology · doi:10.1186/s12915-016-0282-1 · Cited by 62 · see citing works
Bielen, H., Oberleitner, S., Marcellini, S., Gee, L., Lemaire, P., Bode, H. R., Rupp, R., & Technau, U. (2007) · Development · doi:10.1242/dev.010173 · Cited by 61 · see citing works
Self-citationHox, Wnt, and the evolution of the primary body axis: insights from the early-divergent phyla
Ryan, J. F., & Baxevanis, A. D. (2007) · Biology Direct · doi:10.1186/1745-6150-2-37 · Cited by 60 · see citing works
Schaffer, A., Bazarsky, M., Levy, K., Caspi, V. C., & Gat, U. (2016) · BMC Genomics · doi:10.1186/s12864-016-3027-1 · Cited by 58 · see citing works
Molecular insights into the origin of the Hox-TALE patterning system
Hudry, B., Thomas‐Chollier, M., Volovik, Y., Duffraisse, M., Dard, A., Frank, D., Technau, U., & Merabet, S. (2014) · eLife · doi:10.7554/elife.01939 · Cited by 57 · see citing works
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Noordermeer, D., & Duboule, D. (2013) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416027-9.00004-8 · Cited by 54 · see citing works
Moreno, E., Nadal, M., Baguñà, J., & Martı́nez, P. (2009) · Evolution & Development · doi:10.1111/j.1525-142x.2009.00363.x · Cited by 53 · see citing works
The role of cnidarian developmental biology in unraveling axis formation and Wnt signaling
Holstein, T. W. (2022) · Developmental Biology · doi:10.1016/j.ydbio.2022.04.005 · Cited by 51 · see citing works
New tricks with old genes: the genetic bases of novel cnidarian traits
Forêt, S., Knack, B., Houliston, E., Momose, T., Manuel, M., Quéinnec, É., Hayward, D. C., Ball, E. E., & Miller, D. J. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.01.003 · Cited by 51 · see citing works
Mazza, M. E., Pang, K., Reitzel, A. M., Martindale, M. Q., & Finnerty, J. R. (2010) · EvoDevo · doi:10.1186/2041-9139-1-3 · Cited by 51 · see citing works
Genikhovich, G., & Technau, U. (2009) · Cold Spring Harbor Protocols · doi:10.1101/pdb.emo129 · Cited by 51 · see citing works
Self-citationSiegel, N., Hoegg, S., Salzburger, W., Braasch, I., & Meyer, A. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-312 · Cited by 50 · see citing works
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Fritz, A. E., Ikmi, A., Seidel, C. W., Paulson, A., & Gibson, M. C. (2013) · Development · doi:10.1242/dev.088260 · Cited by 45 · see citing works
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Holló, G. (2015) · Interface Focus · doi:10.1098/rsfs.2015.0032 · Cited by 49 · see citing works
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Hajirnis, N., & Mishra, R. K. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.718308 · Cited by 45 · see citing works
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Butts, T., Holland, P. W. H., & Ferrier, D. E. K. (2008) · Trends in Genetics · doi:10.1016/j.tig.2007.09.006 · Cited by 45 · see citing works
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Reddy, P. C., Gungi, A., & Unni, M. (2019) · Results and problems in cell differentiation · doi:10.1007/978-3-030-23459-1_12 · Cited by 44 · see citing works
Kulakova, M. A., Cook, C. E., & Andreeva, T. F. (2008) · BMC Developmental Biology · doi:10.1186/1471-213x-8-61 · Cited by 44 · see citing works
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Schierwater, B., Kamm, K., Srivastava, M., Rokhsar, D. S., Rosengarten, R. D., & Dellaporta, S. L. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002457 · Cited by 44 · see citing works
Olson, P. D. (2007) · Parasitology International · doi:10.1016/j.parint.2007.09.007 · Cited by 43 · see citing works
Shinzato, C., Mungpakdee, S., Satoh, N., & Shoguchi, E. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00336 · Cited by 43 · see citing works
Sikes, J. M., & Bely, A. E. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.10.033 · Cited by 42 · see citing works
NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges
Gazave, E., Lapébie, P., Renard, E., Bézac, C., Boury-Esnault, N., Vacelet, J., Pérez, T., Manuel, M., & Borchiellini, C. (2008) · Development Genes and Evolution · doi:10.1007/s00427-008-0242-z · Cited by 42 · see citing works
Cryptic complexity captured: the Nematostella genome reveals its secrets
Miller, D. J., & Ball, E. E. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.10.002 · Cited by 39 · see citing works
The Precambrian emergence of animal life: a geobiological perspective
Gaidos, E. J., DuBuc, T. Q., Dunford, M. D., MCANDREW, P., PADILLA‐GAMIÑO, J., STUDER, B., Weersing, K., & Stanley, S. M. (2007) · Geobiology · doi:10.1111/j.1472-4669.2007.00125.x · Cited by 38 · see citing works
More constraint on ParaHox than Hox gene families in early metazoan evolution
Quiquand, M., Yanze, N., Schmich, J., Schmid, V. J., Galliot, B., & Piraino, S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.01.022 · Cited by 37 · see citing works
Röttinger, É. (2021) · Cells · doi:10.3390/cells10102692 · Cited by 36 · see citing works
Hui, J. H. L., Holland, P. W. H., & Ferrier, D. E. K. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00286.x · Cited by 36 · see citing works
Wijesena, N. M., Simmons, D. K., & Martindale, M. Q. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1701607114 · Cited by 36 · see citing works
Samadi, L., & Steiner, G. (2010) · BMC Developmental Biology · doi:10.1186/1471-213x-10-74 · Cited by 35 · see citing works
Recent advances in genomics and transcriptomics of cnidarians
Technau, U., & Schwaiger, M. (2015) · Marine Genomics · doi:10.1016/j.margen.2015.09.007 · Cited by 35 · see citing works
Self-citationThomas‐Chollier, M., Ledent, V., Leyns, L., & Vervoort, M. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-73 · Cited by 33 · see citing works
- Authors
- Chourrout, D., Delsuc, F., Chourrout, P., Edvardsen, R. B., Rentzsch, F., Renfer, E., Jensen, M. F., Zhu, B., de Jong, P., Steele, R. E., & Technau, U.
- Affiliations
- University of Bergen (NO)
- Centre National de la Recherche Scientifique (FR)
- Hôpital américain de paris (FR)
- University of California, Irvine (US)
- Corresponding author
- Chourrout, D.
- Technau, U.
- Venue
- Nature
- Published
- 2006-08
- Volume
- 442
- Issue
- 7103
- Pages
- 684-687
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2158564117
- Cited by
- 197
- References
- 21
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 6 · 2023: 7 · 2022: 5 · 2021: 5 · 2020: 5 · 2019: 8 · 2018: 9 · 2017: 4 · 2016: 5 · 2015: 12 · 2014: 11 · 2013: 4 · 2012: 11
- FWCI
- 9.45
- Type
- journal article
- Language
- en
- Open access
- green
- hal.science
- Licence
- other-oa
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- Hox genes, ParaHox genes, gene duplication, Nematostella vectensis, Hydra magnipapillata, Cnidaria, CDX, gene family evolution, genome organization
- MeSH terms
- Animals, Cnidaria, Genes, Homeobox, Multigene Family, Phylogeny, Genome, Homeodomain Proteins, Evolution, Molecular
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