Origins of Bilateral Symmetry: Hox and Dpp Expression in a Sea Anemone
Abstract
Over 99% of modern animals are members of the evolutionary lineage Bilateria. The evolutionary success of Bilateria is credited partly to the origin of bilateral symmetry. Although animals of the phylum Cnidaria are not within the Bilateria, some representatives, such as the sea anemone Nematostella vectensis, exhibit bilateral symmetry. We show that Nematostella uses homologous genes to achieve bilateral symmetry: Multiple Hox genes are expressed in a staggered fashion along its primary body axis, and the transforming growth factor-beta gene decapentaplegic (dpp) is expressed in an asymmetric fashion about its secondary body axis. These data suggest that bilateral symmetry arose before the evolutionary split of Cnidaria and Bilateria.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Cnidarians possess almost the complete bilaterian regulatory gene tool kit, including anterior and posterior hox genes, and generate many differentiated cell types also found in bilaterians.
“Cnidarians seem to possess almost the complete bilaterian regulatory gene tool kit, including anterior and posterior hox genes (Finnerty et al. 2004; Putnam et al. 2007) and generate many of the ectodermal, neuronal, endodermal, and mesodermal differentiated cell types also found in bilaterians.”
From An integrated view of precambrian eumetazoan evolution (2009) · cites this paper as Finnerty et al. 2004
In anthozoans, regulatory genes are expressed in bilateral axial patterns that indicate an underlying set of bilateral regulatory states.
“in development of the most basal cnidarian clade, anthozoans, regulatory genes are expressed in bilateral axial patterns that indicate an underlying set of bilateral regulatory states.”
From An integrated view of precambrian eumetazoan evolution (2009) · cites this paper as Finnerty et al. 2004
Limited conservation of synteny is recognizable within insects, for example between flies and bees.
“Similarly, limited conservation of synteny is recognizable within insects (e.g., between flies and bees (50)).”
From Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization (2007) · cites this paper as [50]
Cites
Animal evolution: interrelationships of the living phyla
(2012) · Choice Reviews Online · doi:10.5860/choice.50-1469 · Cited by 1,041 · see citing works
From DNA to diversity: molecular genetics and the evolution of animal design
Carroll, S., Grenier, J., & Weatherbee, S. D. (2002) · Choice Reviews Online · doi:10.5860/choice.39-5182 · Cited by 986 · see citing works
(1940) · Andalas University Repository (Andalas University) · Cited by 591 · see citing works
Holley, S. A., Jackson, P. D., Sasai, Y., Lu, B., Robertis, E. M. D., Hoffmann, F. M., & Ferguson, E. L. (1995) · Nature · doi:10.1038/376249a0 · Cited by 435 · see citing works
A critical reappraisal of the fossil record of the bilaterian phyla
BUDD, G. E., & JENSEN, S. (2000) · Biological Reviews of the Cambridge Philosophical Society · doi:10.1017/s000632310000548x · Cited by 428 · see citing works
Willmer, P. G. (1990) · Cambridge University Press eBooks · doi:10.1017/cbo9780511623547 · Cited by 323 · see citing works
Invertebrate relationships: patterns in animal evolution
(1990) · Choice Reviews Online · doi:10.5860/choice.28-0957 · Cited by 306 · see citing works
The Late Precambrian fossils from Ediacara, South Australia
Glaessner, M. F., & Wade, M. (1966) · Biodiversity Heritage Library (Smithsonian Institution) · doi:10.5281/zenodo.16238847 · Cited by 290 · see citing works
Principles of Comparative Anatomy of Invertebrates
Willey, R. B., Beklemischev, W. N., MacLennan, J. M., & Kabata, Z. (1971) · Transactions of the American Microscopical Society · doi:10.2307/3225209 · Cited by 274 · 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
Molecular evolution of the homeodomain family of transcription factors
Banerjee‐Basu, S. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.15.3258 · Cited by 186 · 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
Self-citationNEW INVESTIGATIONS ON SYSTEMATICS AND EVOLUTION OF THE CLASS SCYPHOZOA AND THE PHYLUM CNIDARIA
Werner, B. (1973) · Publications of the Seto Marine Biological Laboratory · doi:10.5134/175791 · Cited by 138 · see citing works
Localized expression of a <i>dpp</i> / <i>BMP2</i> / <i>4</i> ortholog in a coral embryo
Hayward, D. C., Samuel, G., Pontynen, P. C., Catmull, J., Saint, R., Miller, D. J., & Ball, E. E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.112021499 · Cited by 132 · see citing works
Conservation of dorsal-ventral patterning in arthropods and chordates
Ferguson, E. L. (1996) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(96)80063-3 · Cited by 117 · see citing works
Hadži, J. (1963) · Macmillan eBooks · doi:10.5962/bhl.title.6821 · Cited by 105 · see citing works
Conservation of Hox/ParaHox-Related Genes in the Early Development of a Cnidarian
Yanze, N., Spring, J., Schmidli, C., & Schmid, V. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0299 · Cited by 99 · see citing works
The evolution of the Hox cluster: insights from outgroups
Finnerty, J. R., & Martindale, M. Q. (1998) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(98)80037-3 · Cited by 92 · see citing works
Self-citationDefining phyla: evolutionary pathways to metazoan body plans
Collins, A. G., & Valentine, J. W. (2001) · Evolution & Development · doi:10.1046/j.1525-142x.2001.01048.x · Cited by 90 · see citing works
Finnerty, J. R., & Martindale, M. Q. (1997) · Biological Bulletin · doi:10.2307/1542736 · Cited by 70 · see citing works
Self-citationBarnes, R. D., & Dougherty, E. C. (1964) · The American Midland Naturalist · doi:10.2307/2423524 · Cited by 70 · 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
Masuda-Nakagawa, L. M., Gröer, H., Aerne, B. L., & Schmid, V. J. (2000) · Development Genes and Evolution · doi:10.1007/s004270050022 · Cited by 51 · see citing works
Combined-method phylogenetic analysis of Hox and ParaHox genes of the metazoa
Kourakis, M. J., & Martindale, M. Q. (2000) · Journal of Experimental Zoology · doi:10.1002/1097-010x(20000815)288:2 · Cited by 51 · see citing works
Self-citationJohnson, G. B. (1994) · Cited by 44 · see citing works
Hatschek, B. (1888) · Cited by 31 · see citing works
Cnidarians Reveal Intermediate Stages in the Evolution of Hox Clusters and Axial Complexity
Finnerty, J. R. (2001) · American Zoologist · doi:10.1093/icb/41.3.608 · Cited by 27 · see citing works
Self-citationTotton, A. K. (1929) · Nature · doi:10.1038/123486a0 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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-citationsurvival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization
Vallortígara, G., & Rogers, L. J. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000105 · Cited by 1,132 · see citing works
Modulating Hox gene functions during animal body patterning
Pearson, J. C., Lemons, D., & McGinnis, W. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1726 · Cited by 879 · see citing works
Phylogenomics Revives Traditional Views on Deep Animal Relationships
Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchiellini, C., Boury-Esnault, N., Vacelet, J., Renard, E., Houliston, E., Quéinnec, E., et al. (2009) · Current Biology · doi:10.1016/j.cub.2009.02.052 · Cited by 695 · see citing works
Unexpected complexity of the Wnt gene family in a sea anemone
Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H. A., Technau, U., von Haeseler, A., Hobmayer, B., Martindale, M. Q., et al. (2005) · Nature · doi:10.1038/nature03158 · Cited by 599 · see citing works
Self-citationWnt Signaling and the Polarity of the Primary Body Axis
Petersen, C. P., & Reddien, P. W. (2009) · Cell · doi:10.1016/j.cell.2009.11.035 · Cited by 544 · see citing works
Explaining the Cambrian "Explosion" of Animals
Marshall, C. R. (2006) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.33.031504.103001 · Cited by 506 · see citing works
The New View of Animal Phylogeny
Halanych, K. M. (2004) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.35.112202.130124 · Cited by 489 · 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 phylum Cnidaria: A review of phylogenetic patterns and diversity 300 years after Linnaeus*
Daly, M., Brugler, M. R., Cartwright, P., Collins, A. G., Dawson, M. N., Fautin, D. G., France, S. C., McFadden, C. S., Opresko, D. M., Rodríguez, E., et al. (2007) · Zootaxa · doi:10.11646/zootaxa.1668.1.11 · Cited by 514 · see citing works
Dorsoventral Patterning in Hemichordates: Insights into Early Chordate Evolution
Lowe, C. J., Terasaki, M., Wu, M., Freeman, R. M., Runft, L., Kwan, K., Haigo, S., Aronowicz, J., Lander, E., Gruber, C., et al. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040291 · Cited by 385 · see citing works
The phylum Cnidaria: A review of phylogenetic patterns and diversity 300 years after Linnaeus *
Daly, M., Brugler, M. R., Cartwright, P., Collins, A. G., Dawson, M. N., Fautin, D. G., France, S. C., McFadden, C. S., Opresko, D. M., Rodríguez, E., et al. (2007) · KU ScholarWorks (The University of Kansas) · doi:10.5281/zenodo.180149 · Cited by 344 · 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
Sempere, L. F., Cole, C. N., McPeek, M. A., & Peterson, K. J. (2006) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21118 · Cited by 307 · see citing works
Genomic Evolution of Hox Gene Clusters
Lemons, D., & McGinnis, W. (2006) · Science · doi:10.1126/science.1132040 · Cited by 385 · see citing works
Niehrs, C. (2010) · Development · doi:10.1242/dev.039651 · Cited by 283 · see citing works
The Ancestral Developmental Tool Kit of Land Plants
Floyd, S. K., & Bowman, J. L. (2006) · International Journal of Plant Sciences · doi:10.1086/509079 · Cited by 289 · 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
The Evolution of Organ Systems
Schmidt‐Rhaesa, A. (2007) · doi:10.1093/acprof:oso/9780198566687.001.0001 · Cited by 262 · see citing works
The evolution and genetics of cerebral asymmetry
Corballis, M. (2009) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2008.0232 · Cited by 289 · see citing works
Kayal, E., Bentlage, B., Sabrina Pankey, M., Ohdera, A. H., Medina, M., Plachetzki, D. C., Collins, A. G., & Ryan, J. F. (2018) · BMC Evolutionary Biology · doi:10.1186/s12862-018-1142-0 · Cited by 255 · see citing works
Marlow, H. Q., Srivastava, M., Matus, D. Q., Rokhsar, D., & Martindale, M. Q. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20698 · Cited by 247 · see citing works
Self-citationCnidarian phylogenetic relationships as revealed by mitogenomics
Kayal, E., Roure, B., Philippe, H., Collins, A. G., & Lavrov, D. V. (2013) · BMC Evolutionary Biology · doi:10.1186/1471-2148-13-5 · Cited by 240 · 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
Self-citationAncient Venom Systems: A Review on Cnidaria Toxins
Jouiaei, M., Yanagihara, A. A., Madio, B., Nevalainen, T. J., Alewood, P. F., & Fry, B. G. (2015) · Toxins · doi:10.3390/toxins7062251 · Cited by 240 · see citing works
Molecular evidence for deep evolutionary roots of bilaterality in animal development
Matus, D. Q., Pang, K., Marlow, H. Q., Dunn, C. W., Thomsen, G. H., & Martindale, M. Q. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601257103 · Cited by 227 · see citing works
Self-citationOn the Independent Origins of Complex Brains and Neurons
Moroz, L. L. (2009) · Brain, Behavior and Evolution · doi:10.1159/000258665 · Cited by 209 · 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
Self-citationCnidarians 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
The evolution of metazoan axial properties
Martindale, M. Q. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1725 · Cited by 204 · see citing works
Self-citationExceptionally Preserved Jellyfishes from the Middle Cambrian
Cartwright, P., Halgedahl, S. L., Hendricks, J. R., Jarrard, R. D., Marques, A. C., Collins, A. G., & Lieberman, B. S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001121 · Cited by 210 · see citing works
Lapraz, F., Besnardeau, L., & Lepage, T. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000248 · Cited by 202 · see citing works
Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements
Chourrout, D., Delsuc, F., Chourrout, P., Edvardsen, R. B., Rentzsch, F., Renfer, E., Jensen, M. F., Zhu, B., de Jong, P., Steele, R. E., et al. (2006) · Nature · doi:10.1038/nature04863 · Cited by 197 · 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
Sperling, E. A., & Vinther, J. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00404.x · Cited by 194 · see citing works
Nakanishi, N., Renfer, E., Technau, U., & Rentzsch, F. (2012) · Development · doi:10.1242/dev.071902 · Cited by 188 · see citing works
A WNT of things to come: Evolution of Wnt signaling and polarity in cnidarians
LEE, P., PANG, K., Matus, D. Q., & Martindale, M. Q. (2006) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2006.05.002 · Cited by 185 · see citing works
Self-citationRyan, J. F., Burton, P. M., Mazza, M. E., Kwong, G. K., Mullikin, J. C., & Finnerty, J. R. (2006) · Genome biology · doi:10.1186/gb-2006-7-7-r64 · Cited by 185 · 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
Buddenbrockia Is a Cnidarian Worm
Jiménez-Guri, E., Philippe, H., Okamura, B., & Holland, P. W. H. (2007) · Science · doi:10.1126/science.1142024 · Cited by 175 · see citing works
Tempo and mode of early animal evolution: inferences from rocks, Hox, and molecular clocks
Peterson, K. J., McPeek, M. A., & Evans, D. A. D. (2005) · Paleobiology · doi:10.1666/0094-8373(2005)031[0036:tamoea]2.0.co;2 · Cited by 173 · 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
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
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
Rentzsch, 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
The Bilaterian Head Patterning Gene six3/6 Controls Aboral Domain Development in a Cnidarian
Sinigaglia, C., Busengdal, H., Leclère, L., Technau, U., & Rentzsch, F. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001488 · Cited by 169 · see citing works
The Evolutionary History of YAP and the Hippo/YAP Pathway
Hilman, D., & Gat, U. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr065 · Cited by 166 · see citing works
Acoel 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
Self-citationGenomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis
Magie, C. R., Pang, K., & Martindale, M. Q. (2005) · Development Genes and Evolution · doi:10.1007/s00427-005-0022-y · Cited by 158 · see citing works
Self-citationLayden, M. J., Rentzsch, F., & Röttinger, É. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.222 · Cited by 148 · see citing works
Early origin of the bilaterian developmental toolkit
Erwin, D. H. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0038 · Cited by 154 · see citing works
Dual-Gel 4D Printing of Bioinspired Tubes
Liu, J., Erol, O., Pantula, A., Liu, W., Jiang, Z., Kobayashi, K., Chatterjee, D., Hibino, N., Romer, L. H., Kang, S. H., et al. (2019) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.8b17218 · Cited by 156 · see citing works
Phylogenomics, Origin, and Diversification of Anthozoans (Phylum Cnidaria)
McFadden, C. S., Quattrini, A. M., Brugler, M. R., Cowman, P. F., Dueñas, L. F., Kitahara, M. V., Paz‐García, D. A., Reimer, J. D., & Rodríguez, E. (2020) · Systematic Biology · doi:10.1093/sysbio/syaa103 · Cited by 155 · see citing works
RTK and TGF-β signaling pathways genes in the sea urchin genome
Lapraz, F., Röttinger, É., Duboc, V., Range, R., Duloquin, L., Walton, K. D., Wu, S.-Y., Bradham, C. A., Loza‐Coll, M., Hibino, T., et al. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.08.048 · Cited by 153 · 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
Beyond bilateral symmetry: geometric morphometric methods for any type of symmetry
Savriama, Y., & Klingenberg, C. P. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-280 · Cited by 146 · 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
Vogt, G. (2015) · Journal of Biosciences · doi:10.1007/s12038-015-9506-8 · Cited by 141 · see citing works
The phylogenetic position of the comb jellies (Ctenophora) and the importance of taxonomic sampling
Wållberg, A., Thollesson, M., Farris, J. S., & Jondelius, U. (2004) · Cladistics · doi:10.1111/j.1096-0031.2004.00041.x · Cited by 141 · see citing works
Röttinger, E., Dahlin, P., & Martindale, M. Q. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003164 · Cited by 140 · see citing works
Self-citationBMPs and Chordin regulate patterning of the directive axis in a sea anemone
Saina, M., Genikhovich, G., Renfer, E., & Technau, U. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900151106 · Cited by 138 · see citing works
Hox, ParaHox, ProtoHox: facts and guesses
García‐Fernàndez, J. (2004) · Heredity · doi:10.1038/sj.hdy.6800621 · Cited by 138 · 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
Lee, P. N., Kumburegama, S., Marlow, H. Q., Martindale, M. Q., & Wikramanayake, A. H. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.05.040 · Cited by 135 · see citing works
Self-citationMatus, D. Q., Magie, C. R., Pang, K., Martindale, M. Q., & Thomsen, G. H. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.09.032 · Cited by 134 · see citing works
Self-citationSchnitzler, C. E., Pang, K., Powers, M. L., Reitzel, A. M., Ryan, J. F., Simmons, D., Tada, T., Park, M., Gupta, J., Brooks, S. Y., et al. (2012) · BMC Biology · doi:10.1186/1741-7007-10-107 · Cited by 132 · see citing works
Self-citationA Developmental Perspective: Changes in the Position of the Blastopore during Bilaterian Evolution
Martindale, M. Q., & Hejnol, A. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.07.024 · Cited by 130 · see citing works
Self-citationMatus, D. Q., Thomsen, G. H., & Martindale, M. Q. (2006) · Current Biology · doi:10.1016/j.cub.2006.01.052 · Cited by 129 · see citing works
Self-citationTautz, D. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.08.008 · Cited by 127 · see citing works
A simple plan-Cnidarians and the origins of developmental mechanisms
Ball, E. E., Hayward, D. C., Saint, R., & Miller, D. J. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1402 · Cited by 123 · see citing works
Cnidarians and ancestral genetic complexity in the animal kingdom
Miller, D. J., Ball, E. E., & Technau, U. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.08.002 · Cited by 124 · see citing works
Clytia hemisphaerica: a jellyfish cousin joins the laboratory
Houliston, E., Momose, T., & Manuel, M. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.01.008 · Cited by 119 · 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
Are we there yet? Tracking the development of new model systems
Abzhanov, A., Extavour, C. G. M., Groover, A. T., Hodges, S. A., Hoekstra, H. E., Kramer, E. M., & Monteiro, A. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.04.002 · Cited by 121 · see citing works
Axial Patterning and Diversification in the Cnidaria Predate the Hox System
Kamm, K., Schierwater, B., Jakob, W., Dellaporta, S. L., & Miller, D. J. (2006) · Current Biology · doi:10.1016/j.cub.2006.03.036 · Cited by 118 · 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
Axis Patterning by BMPs: Cnidarian Network Reveals Evolutionary Constraints
Genikhovich, G., Fried, P., Prünster, M. M., Schinko, J. B., Gilles, A. F., Fredman, D., Meier, K., Iber, D., & Technau, U. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.035 · Cited by 113 · see citing works
EvoD/Vo: the origins of BMP signalling in the neuroectoderm
Mizutani, C. M., & Bier, E. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2417 · Cited by 113 · see citing works
Cnidarian 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
Kraus, Y. A., & Technau, U. (2006) · Development Genes and Evolution · doi:10.1007/s00427-005-0038-3 · Cited by 104 · see citing works
StellaBase: The Nematostella vectensis Genomics Database
Sullivan, J. C. (2005) · Nucleic Acids Research · doi:10.1093/nar/gkj020 · Cited by 108 · see citing works
Back 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
Transcriptome profiling of the dynamic life cycle of the scypohozoan jellyfish Aurelia aurita
Brekhman, V., Malik, A., Haas, B. J., Sher, N., & Lotan, T. (2015) · BMC Genomics · doi:10.1186/s12864-015-1320-z · Cited by 101 · see citing works
Bone Morphogenetic Protein (BMP) signaling in animal reproductive system development and function
Lochab, A. K., & Extavour, C. G. M. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.03.002 · Cited by 102 · see citing works
Functional roles of Notch signaling in the cnidarian Nematostella vectensis
Marlow, H. Q., Röttinger, É., Boekhout, M., & Martindale, M. Q. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.11.012 · Cited by 101 · see citing works
Self-citationThe vertebrate heart: an evolutionary perspective
Stephenson, A., Adams, J. W., & Vaccarezza, M. (2017) · Journal of Anatomy · doi:10.1111/joa.12687 · Cited by 101 · see citing works
Goldstone, J. V. (2008) · Cell Biology and Toxicology · doi:10.1007/s10565-008-9107-5 · 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
Nielsen, C. (2005) · Evolution & Development · doi:10.1111/j.1525-142x.2005.05051.x · Cited by 95 · see citing works
Evolution of the TGF-β Signaling Pathway and Its Potential Role in the Ctenophore, Mnemiopsis leidyi
Pang, K., Ryan, J. F., Baxevanis, A. D., & Martindale, M. Q. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024152 · Cited by 93 · see citing works
Self-citationMcGregor, A. P., Hilbrant, M., Pechmann, M., Schwager, E. E., Prpíc, N.-M., & Damen, W. G. M. (2008) · BioEssays · doi:10.1002/bies.20744 · Cited by 93 · see citing works
Corballis, M. C., Badzakova‐Trajkov, G., & Häberling, I. S. (2011) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.158 · Cited by 93 · see citing works
Sequential actions of β-catenin and Bmp pattern the oral nerve net in Nematostella vectensis
Watanabe, H., Kuhn, A., Fushiki, M., Agata, K., Özbek, S., Fujisawa, T., & Holstein, T. W. (2014) · Nature Communications · doi:10.1038/ncomms6536 · Cited by 79 · see citing works
Phylogenetic evidence for the modular evolution of metazoan signalling pathways
Babonis, L. S., & Martindale, M. Q. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0477 · Cited by 86 · see citing works
Self-citationEvolution of sensory structures in basal metazoa
Jacobs, D. K., Nakanishi, N., Yuan, D., Camara, A., Nichols, S., & Hartenstein, V. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm094 · Cited by 87 · see citing works
Plickert, G., Frank, U., & Müller, W. A. (2012) · The International Journal of Developmental Biology · doi:10.1387/ijdb.123502gp · Cited by 86 · see citing works
Xu, X., Li, G., Li, C., Zhang, J., Wang, Q., Simmons, D. K., Chen, X., Wijesena, N. M., Zhu, W. Z., Wang, Z., et al. (2019) · National Science Review · doi:10.1093/nsr/nwz064 · Cited by 82 · see citing works
Self-citationWindsor, P. J., & Leys, S. P. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00434.x · Cited by 84 · see citing works
- Authors
- Finnerty, J. R., Pang, K., Burton, P., Paulson, D., & Martindale, M. Q.
- Affiliations
- Boston University (US)
- Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215, USA.
- Corresponding author
- Finnerty, John R.
- Venue
- Science
- Published
- 2004-05-28
- Volume
- 304
- Issue
- 5675
- Pages
- 1335-1337
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2030545022
- Cited by
- 407
- References
- 28
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 14 · 2023: 6 · 2022: 16 · 2021: 11 · 2020: 6 · 2019: 16 · 2018: 12 · 2017: 11 · 2016: 14 · 2015: 24 · 2014: 18 · 2013: 10 · 2012: 16
- FWCI
- 16.02
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
- Keywords
- bilateral symmetry, Nematostella vectensis, sea anemone, Hox genes, decapentaplegic, DPP, TGF-beta, body axis patterning, Cnidaria, homologous genes
- MeSH terms
- Amino Acid Sequence, Animals, Endoderm, Genes, Genes, Homeobox, Larva, Molecular Sequence Data, Phylogeny, Sea Anemones, In Situ Hybridization, Gene Expression Regulation, Developmental, Body Patterning, Gene Duplication, Gene Expression Profiling
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
