Dorsoventral Patterning in Hemichordates: Insights into Early Chordate Evolution
Open accessAbstract
We have compared the dorsoventral development of hemichordates and chordates to deduce the organization of their common ancestor, and hence to identify the evolutionary modifications of the chordate body axis after the lineages split. In the hemichordate embryo, genes encoding bone morphogenetic proteins (Bmp) 2/4 and 5/8, as well as several genes for modulators of Bmp activity, are expressed in a thin stripe of ectoderm on one midline, historically called "dorsal." On the opposite midline, the genes encoding Chordin and Anti-dorsalizing morphogenetic protein (Admp) are expressed. Thus, we find a Bmp-Chordin developmental axis preceding and underlying the anatomical dorsoventral axis of hemichordates, adding to the evidence from Drosophila and chordates that this axis may be at least as ancient as the first bilateral animals. Numerous genes encoding transcription factors and signaling ligands are expressed in the three germ layers of hemichordate embryos in distinct dorsoventral domains, such as pox neuro, pituitary homeobox, distalless, and tbx2/3 on the Bmp side and netrin, mnx, mox, and single-minded on the Chordin-Admp side. When we expose the embryo to excess Bmp protein, or when we deplete endogenous Bmp by small interfering RNA injections, these expression domains expand or contract, reflecting their activation or repression by Bmp, and the embryos develop as dorsalized or ventralized limit forms. Dorsoventral patterning is independent of anterior/posterior patterning, as in Drosophila but not chordates. Unlike both chordates and Drosophila, neural gene expression in hemichordates is not repressed by high Bmp levels, consistent with their development of a diffuse rather than centralized nervous system. We suggest that the common ancestor of hemichordates and chordates did not use its Bmp-Chordin axis to segregate epidermal and neural ectoderm but to pattern many other dorsoventral aspects of the germ layers, including neural cell fates within a diffuse nervous system. Accordingly, centralization was added in the chordate line by neural-epidermal segregation, mediated by the pre-existing Bmp-Chordin axis. Finally, since hemichordates develop the mouth on the non-Bmp side, like arthropods but opposite to chordates, the mouth and Bmp-Chordin axis may have rearranged in the chordate line, one relative to the other.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
In annelids and hemichordates, Bmp treatments did not inhibit early neurogenic gene expression.
“In annelids22 and in hemichordates24, Bmp treatments did not inhibit early neurogenic gene expression.”
From Sequential actions of β-catenin and Bmp pattern the oral nerve net in Nematostella vectensis (2014) · cites this paper as [24]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Coffinier, C., Ketpura, N. I., Tran, U., Geissert, D., & Robertis, E. M. D. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(03)00113-8 · Cited by 56 · see citing works
RetractedMicroscopic anatomy of invertebrates
Harrison, F. W. (1991) · Wiley-Liss eBooks · Cited by 2,736 · see citing works
Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A., & McMahon, A. P. (1993) · Cell · doi:10.1016/0092-8674(93)90627-3 · Cited by 2,154 · see citing works
Neuronal specification in the spinal cord: inductive signals and transcriptional codes
Jessell, T. M. (2000) · Nature Reviews Genetics · doi:10.1038/35049541 · Cited by 2,089 · see citing works
Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord
Kennedy, T. E., Serafini, T. A., de la Torre, J. R., & Tessier‐Lavigne, M. (1994) · Cell · doi:10.1016/0092-8674(94)90421-9 · Cited by 1,341 · see citing works
Netrin-1 Is Required for Commissural Axon Guidance in the Developing Vertebrate Nervous System
Serafini, T. A., Colamarino, S. A., Leonardo, E. D., Wang, H., Beddington, R. S. P., Skarnes, W. C., & Tessier‐Lavigne, M. (1996) · Cell · doi:10.1016/s0092-8674(00)81795-x · Cited by 1,286 · see citing works
Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm
Liem, K. F., Tremml, G., Roelink, H., & Jessell, T. M. (1995) · Cell · doi:10.1016/0092-8674(95)90276-7 · Cited by 1,071 · see citing works
Structure and function in the nervous systems of invertebrates
Bullock, T. H., Horridge, G. A., Bern, H. A., Hagedorn, I. R., & Smith, J. E. (1965) · Cited by 1,042 · see citing works
Structure and function in the nervous systems of invertebrates
Young, J. Z. (1966) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(66)90114-3 · Cited by 945 · see citing works
Lu, Q. R., Yuk, D.-I., Alberta, J., Zhu, Z.-M., Pawlitzky, I., Chan, J., McMahon, A., Stiles, C., & Rowitch, D. H. (2000) · Neuron · doi:10.1016/s0896-6273(00)80897-1 · Cited by 883 · see citing works
Roelink, H., Augsburger, A., Heemskerk, J., Korzh, V. P., Norlin, S., Altaba, A. R. I., Tanabe, Y., Placzek, M., Edlund, H., Jessell, T. M., et al. (1994) · Cell · doi:10.1016/0092-8674(94)90514-2 · Cited by 854 · see citing works
Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks
Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jónsson, B., Schluter, D., & Kingsley, D. M. (2004) · Nature · doi:10.1038/nature02415 · Cited by 843 · see citing works
A common plan for dorsoventral patterning in Bilateria
De Robertis, E. M., & Sasai, Y. (1996) · Nature · doi:10.1038/380037a0 · Cited by 780 · see citing works
Microscopic Anatomy of Invertebrates
GHIRADELLA, H. T. (1998) · Medical Entomology and Zoology · Cited by 775 · see citing works
Silencing of TGF-β signalling by the pseudoreceptor BAMBI
Onichtchouk, D., Chen, Y., Dosch, R., Gawantka, V., Delius, H., Massagué, J., & Niehrs, C. (1999) · Nature · doi:10.1038/46794 · Cited by 727 · see citing works
DORSAL-VENTRAL PATTERNING AND NEURAL INDUCTION IN <i>XENOPUS</i> EMBRYOS
De Robertis, E. M., & Kuroda, H. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.011403.154124 · Cited by 671 · see citing works
Rossi, J. M., Dunn, N. R., Hogan, B. L. M., & Zaret, K. S. (2001) · Genes & Development · doi:10.1101/gad.904601 · Cited by 646 · see citing works
Requirement for the Homeobox Gene Hb9 in the Consolidation of Motor Neuron Identity
Arber, S., Han, B., Mendelsohn, M. M., Smith, M., Jessell, T. M., & Sockanathan, S. (1999) · Neuron · doi:10.1016/s0896-6273(01)80026-x · Cited by 607 · see citing works
Self-citationSpecification of neuronal fates in the ventral neural tube
Briscoe, J., & Ericson, J. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00172-0 · Cited by 548 · see citing works
Anteroposterior patterning in hemichordates and the origins of the chordate nervous system
Lowe, C. J., Wu, M., Salic, A., Evans, L., Lander, E., Stange-Thomann, N., Gruber, C. E., Gerhart, J., & Kirschner, M. (2003) · Cell · doi:10.1016/s0092-8674(03)00469-0 · Cited by 531 · see citing works
Self-citationKishimoto, Y., Lee, K., Zon, L. I., Hammerschmidt, M., & Schulte‐Merker, S. (1997) · Development · doi:10.1242/dev.124.22.4457 · Cited by 520 · see citing works
Nambu, J. R., Lewis, J. O., Wharton, K. A., & Crews, S. T. (1991) · Cell · doi:10.1016/0092-8674(91)90292-7 · Cited by 493 · see citing works
Martı́nez-Barberá, J. P., Clements, M., Thomas, P. Q., Rodríguez, T. A., Meloy, D., Kioussis, D., & Beddington, R. S. P. (2000) · Development · doi:10.1242/dev.127.11.2433 · Cited by 474 · see citing works
Synexpression groups in eukaryotes
Niehrs, C., & Pollet, N. (1999) · Nature · doi:10.1038/990025 · Cited by 440 · 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
Vertebrate Embryonic Cells Will Become Nerve Cells Unless Told Otherwise
Hemmati‐Brivanlou, A., & Melton, D. A. (1997) · Cell · doi:10.1016/s0092-8674(00)81853-x · Cited by 364 · see citing works
Marqués, G., Musacchio, M., Shimell, M., Wünnenberg-Stapleton, K., Cho, K. W. Y., & O’Connor, M. B. (1997) · Cell · doi:10.1016/s0092-8674(00)80425-0 · Cited by 349 · see citing works
Inversion of dorsoventral axis?
Arendt, D., & Nübler‐Jung, K. (1994) · Nature · doi:10.1038/371026a0 · Cited by 334 · see citing works
Harris, R. L., Sabatelli, L. M., & Seeger, M. A. (1996) · Neuron · doi:10.1016/s0896-6273(00)80154-3 · Cited by 328 · see citing works
Short- and Long-Range Repulsion by the Drosophila Unc5 Netrin Receptor
Keleman, K., & Dickson, B. J. (2001) · Neuron · doi:10.1016/s0896-6273(01)00505-0 · Cited by 314 · see citing works
Twisted gastrulation is a conserved extracellular BMP antagonist
Ross, J. J., Shimmi, O., Vilmos, P., Petryk, A., Kim, H., Gaudenz, K., Hermanson, S., Ekker, S. C., O’Connor, M. B., & Marsh, J. L. (2001) · Nature · doi:10.1038/35068578 · Cited by 302 · see citing works
Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition
Delaune, E. A., Lemaire, P., & Kodjabachian, L. (2004) · Development · doi:10.1242/dev.01582 · Cited by 290 · see citing works
The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling
Oelgeschläger, M., Larraı́n, J., Geissert, D., & Robertis, E. M. D. (2000) · Nature · doi:10.1038/35015500 · Cited by 279 · see citing works
Left-Right Asymmetry in the Sea Urchin Embryo Is Regulated by Nodal Signaling on the Right Side
Duboc, V., Röttinger, É., Lapraz, F., Besnardeau, L., & Lepage, T. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.05.008 · Cited by 274 · see citing works
Timmer, J. R., Wang, C. I., & Niswander, L. A. (2002) · Development · doi:10.1242/dev.129.10.2459 · Cited by 255 · see citing works
Early central nervous system evolution: an era of skin brains?
Holland, N. D. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1175 · Cited by 250 · see citing works
Reversade, B., & Robertis, E. M. D. (2005) · Cell · doi:10.1016/j.cell.2005.08.047 · Cited by 248 · see citing works
Yamada, M., Revelli, J., Eichele, G., Barron, M., & Schwartz, R. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9927 · Cited by 228 · see citing works
Control of the Gene optomotor-blind in Drosophila Wing Development by decapentaplegic and wingless
Grimm, S., & Pflugfelder, G. O. (1996) · Science · doi:10.1126/science.271.5255.1601 · Cited by 205 · see citing works
Twisted gastrulation can function as a BMP antagonist
Chang, C., Holtzman, D. A., Chau, S., Chickering, T. W., Woolf, E. A., Holmgren, L. M., Bodorova, J., Gearing, D. P., Holmes, W. E., & Brivanlou, A. H. (2001) · Nature · doi:10.1038/35068583 · Cited by 202 · see citing works
Kuroda, H., Wessely, O., & Robertis, E. M. D. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020092 · Cited by 195 · see citing works
Cleavage of the BMP-4 Antagonist Chordin by Zebrafish Tolloid
Blader, P., Rastegar, S., Fischer, N., & Strähle, U. (1997) · Science · doi:10.1126/science.278.5345.1937 · Cited by 190 · see citing works
Xenoturbella is a deuterostome that eats molluscs
Bourlat, S. J., Nielsen, C., Lockyer, A. E., Littlewood, D. T. J., & Telford, M. J. (2003) · Nature · doi:10.1038/nature01851 · Cited by 188 · see citing works
Local inhibition and long-range enhancement of Dpp signal transduction by Sog
Ashe, H. L., & Levine, M. (1999) · Nature · doi:10.1038/18892 · Cited by 183 · see citing works
Divergent roles for NK-2 class homeobox genes in cardiogenesis in flies and mice
Ranganayakulu, G., Elliott, D. A., Harvey, R. P., & Olson, E. N. (1998) · Development · doi:10.1242/dev.125.16.3037 · Cited by 182 · see citing works
Biehs, B., François, V., & Bier, E. (1996) · Genes & Development · doi:10.1101/gad.10.22.2922 · Cited by 178 · see citing works
Brachyury-Related Transcription Factor Tbx2 and Repression of the Melanocyte-Specific TRP-1 Promoter
Carreira, S., Dexter, T. J., Yavuzer, U., Easty, D. J., & Goding, C. R. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.9.5099 · Cited by 173 · see citing works
The role of chordin/Bmp signals in mammalian pharyngeal development and DiGeorge syndrome
Bachiller, D., Klingensmith, J., Shneyder, N., Tran, U., Anderson, R. M., Rossant, J., & Robertis, E. M. D. (2003) · Development · doi:10.1242/dev.00581 · Cited by 167 · see citing works
Multiple functions of Dlx genes
Merlo, G. R., Zerega, B., Paleari, L., Trombino, S., Mantero, S., & Levi, G. (2000) · The International Journal of Developmental Biology · doi:10.1387/ijdb.11061425 · Cited by 162 · see citing works
Vnd/nkx, ind/gsh, and msh/msx: conserved regulators of dorsoventral neural patterning?
Cornell, R. A., & Ohlen, T. L. V. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00049-5 · Cited by 161 · see citing works
Conley, C. A., Silburn, R., Singer, M. A., Ralston, A., Rohwer-Nutter, D., Olson, D. J., Gelbart, W. M., & Blair, S. S. (2000) · Development · doi:10.1242/dev.127.18.3947 · Cited by 160 · see citing works
Transcriptional regulation of BMP4 synexpression in transgenic Xenopus
Karaulanov, E., Knöchel, W., & Niehrs, C. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600101 · Cited by 158 · see citing works
The evolution of the hedgehog gene family in chordates: insights from amphioxus hedgehog
Shimeld, S. M. (1999) · Development Genes and Evolution · doi:10.1007/s004270050225 · Cited by 156 · see citing works
Lichtneckert, R., & Reichert, H. (2005) · Heredity · doi:10.1038/sj.hdy.6800664 · Cited by 153 · see citing works
The paired box gene pox neuro: A determiant of poly-innervated sense organs in Drosophila
Dambly‐Chaudière, C., Jamet, É., Burri, M., Bopp, D., Basler, K., Hafen, E., Dumont, N., Spielmann, P., Ghysen, A., & Noll, M. (1992) · Cell · doi:10.1016/0092-8674(92)90127-x · Cited by 139 · see citing works
Regulation of motor neuron subtype identity by repressor activity of Mnx class homeodomain proteins
William, C., Tanabe, Y., & Jessell, T. (2003) · Development · doi:10.1242/dev.00358 · Cited by 136 · see citing works
Ohlen, T. L. V., & Doe, C. Q. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9789 · Cited by 136 · see citing works
Biphasic activation of the BMP pathway patterns the Drosophila embryonic dorsal region
Dorfman, R., & Shilo, B. (2001) · Development · doi:10.1242/dev.128.6.965 · Cited by 128 · see citing works
The development of balanoglossus
Morgan, T. H. (1894) · Journal of Morphology · doi:10.1002/jmor.1050090102 · Cited by 124 · see citing works
Distinct activities of Msx1 and Msx3 in dorsal neural tube development
Liu, Y. M., Helms, A. W., & Johnson, J. E. B. (2004) · Development · doi:10.1242/dev.00994 · Cited by 122 · see citing works
Darras, S., & Nishida, H. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0339 · Cited by 121 · 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
Bambi is coexpressed with Bmp-4 during mouse embryogenesis
Grotewold, L., Plum, M., Dildrop, R., Peters, T., & Rüther, U. (2001) · Mechanisms of Development · doi:10.1016/s0925-4773(00)00524-4 · Cited by 114 · see citing works
Hemichordates and the origin of chordates
Gerhart, J. C., Lowe, C. J., & Kirschner, M. W. (2005) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2005.06.004 · Cited by 113 · see citing works
Self-citationSkeath, J. B. (1998) · Development · doi:10.1242/dev.125.17.3301 · Cited by 111 · see citing works
The Radiata and the evolutionary origins of the bilaterian body plan
Martindale, M. Q., Finnerty, J. R., & Henry, J. Q. (2002) · Molecular Phylogenetics and Evolution · doi:10.1016/s1055-7903(02)00208-7 · Cited by 110 · see citing works
Rentzsch, F., Zhang, J., Kramer, C., Sebald, W., & Hammerschmidt, M. (2006) · Development · doi:10.1242/dev.02250 · Cited by 107 · see citing works
Balser, E. J., & Ruppert, E. E. (1990) · Acta Zoologica · doi:10.1111/j.1463-6395.1990.tb01082.x · Cited by 104 · see citing works
Brickman, J. M., Jones, C. M., Clements, M., Smith, J. C., & Beddington, R. S. P. (2000) · Development · doi:10.1242/dev.127.11.2303 · Cited by 100 · see citing works
Hemichordate Embryos: Procurement, Culture, and Basic Methods
Lowe, C. J., Tagawa, K., Humphreys, T., Kirschner, M. W., & Gerhart, J. C. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)74008-x · Cited by 99 · see citing works
Self-citationQuantitative Microinjection of Oocytes, Eggs, and Embryos
Jaffe, L. A., & Terasaki, M. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)74010-8 · Cited by 93 · see citing works
Self-citationBateson, W. (1885) · Journal of Cell Science · doi:10.1242/jcs.s2-25.s1.81 · Cited by 92 · see citing works
Sun, H., Rodin, A. S., Zhou, Y., Dickinson, D. P., Harper, D. E., Hewett‐Emmett, D., & Li, W. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.10.5156 · Cited by 85 · see citing works
Conserved and divergent expression of T-box genes Tbx2-Tbx5 in Xenopus
Takabatake, Y., Takabatake, T., & Takeshima, K. (2000) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00329-9 · Cited by 84 · see citing works
Holland, N. D., Venkatesh, T. V., Holland, L. Z., Jacobs, D. K., & Bodmer, R. (2003) · Developmental Biology · doi:10.1016/s0012-1606(02)00050-7 · Cited by 80 · see citing works
Human Crossveinless-2 is a novel inhibitor of bone morphogenetic proteins
Binnerts, M. E., Wen, X., Canté-Barrett, K., Bright, J. M., Chen, H.-T., Asundi, V. K., Sattari, P., Tang, T., Boyle, B., Funk, W. D., et al. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.01.048 · Cited by 76 · see citing works
The Evolution of Chordate Neural Segmentation
Mazet, F., & Shimeld, S. M. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0831 · Cited by 73 · see citing works
Conduction pathways in the nervous system ofSaccoglossussp. (Enteropneusta)
Cameron, C. B., & Mackie, G. O. (1996) · Canadian Journal of Zoology · doi:10.1139/z96-003 · Cited by 72 · see citing works
Pitx genes in Tunicates provide new molecular insight into the evolutionary origin of pituitary
Christiaen, L., Burighel, P., Smith, W. C., Vernier, P., Bourrat, F., & Joly, J. (2002) · Gene · doi:10.1016/s0378-1119(01)00865-4 · Cited by 70 · see citing works
Gross, J. M., Peterson, R. E., Wu, S.-Y., & McClay, D. R. (2003) · Development · doi:10.1242/dev.00409 · Cited by 65 · see citing works
Enteropneusts and chordate evolution
Nübler‐Jung, K., & Arendt, D. (1996) · Current Biology · doi:10.1016/s0960-9822(02)00491-8 · Cited by 64 · see citing works
The Mnx homeobox gene class defined by HB9 , MNR2 and amphioxus AmphiMnx
Ferrier, D. E. K., Brooke, N. M., Panopoulou, G., & Holland, P. W. H. (2001) · Development Genes and Evolution · doi:10.1007/s004270000124 · Cited by 56 · see citing works
Lele, Z., Nowak, M., & Hammerschmidt, M. (2001) · Developmental Dynamics · doi:10.1002/dvdy.1222 · Cited by 55 · see citing works
The normal embryology of saccoglossus kowalevskii (enteropneusta)
Colwin, A. L., & Colwin, L. H. (1953) · Journal of Morphology · doi:10.1002/jmor.1050920302 · Cited by 54 · see citing works
The anatomical organization of the nervous system of Enteropneusta.
Bullock, T. H. (1945) · PubMed · Cited by 53 · see citing works
Goodrich, E. S. (1917) · Journal of Cell Science · doi:10.1242/jcs.s2-62.248.539 · Cited by 53 · see citing works
Filippi, A., Tiso, N., Deflorian, G., Zecchin, E., Bortolussi, M., & Argenton, F. (2005) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0407284102 · Cited by 46 · see citing works
Origin and evolution of the neural crest: A hypothetical reconstruction of its evolutionary history
Wada, H. (2001) · Development Growth & Differentiation · doi:10.1046/j.1440-169x.2001.00600.x · Cited by 45 · see citing works
The Early Stages in the Development of Balanoglossus (sp. incert.)
Bateson, W. (1884) · Journal of Cell Science · doi:10.1242/jcs.s2-24.94.208 · Cited by 42 · see citing works
Characterization ofmsim,a Murine Homologue of theDrosophila simTranscription Factor
Moffett, P., Dayo, M., Reece, M., McCormick, M. K., & Pelletier, J. (1996) · Genomics · doi:10.1006/geno.1996.0333 · Cited by 36 · see citing works
Hinman, V. F., & Degnan, B. M. (2002) · Development Genes and Evolution · doi:10.1007/s00427-002-0223-6 · Cited by 34 · see citing works
Minguillón, C., & García‐Fernàndez, J. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0660 · Cited by 33 · see citing works
Holland, L. Z., Venkatesh, T. V., Gorlin, A., Bodmer, R., & Holland, N. D. (1998) · Development Genes and Evolution · doi:10.1007/s004270050159 · Cited by 32 · see citing works
An amphioxus netrin gene is expressed in midline structures during embryonic and larval development
Shimeld, S. M. (2000) · Development Genes and Evolution · doi:10.1007/s004270000073 · Cited by 32 · see citing works
Rusten, T. E., Cantera, R., Kafatos, F. C., & Barrio, R. (2002) · Development · doi:10.1242/dev.129.15.3575 · Cited by 32 · see citing works
Colwin, A. L., & Colwin, L. H. (1950) · Journal of Experimental Zoology · doi:10.1002/jez.1401150204 · Cited by 29 · see citing works
Bateson, W. (1886) · Journal of Cell Science · doi:10.1242/jcs.s2-26.104.511 · Cited by 28 · see citing works
Expression of Xenopus T-box transcription factor, Tbx2 in Xenopus embryo
Hayata, T., Kuroda, H., Eisaki, A., & Asashima, M. (1999) · Development Genes and Evolution · doi:10.1007/s004270050297 · Cited by 23 · see citing works
Induction of spawning in Saccoglossus kowalevskii (Enteropneusta) at Woods Hole
Colwin, A. (1962) · Biological Bulletin · Cited by 17 · see citing works
Coumailleau, P., Penrad‐Mobayed, M., Boulangé-Lecomte, C., Bollérot, K., Simon, F., Poellinger, L., & Angelier, N. (2000) · Mechanisms of Development · doi:10.1016/s0925-4773(00)00468-8 · Cited by 16 · see citing works
Hara, Y., & Katow, H. (2005) · Gene Expression Patterns · doi:10.1016/j.modgep.2004.12.003 · Cited by 15 · see citing works
Choosing among Alternative Trees of Multigene Families
Martin, A. P. (2000) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.2000.0818 · Cited by 10 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Hyman LH (1940) The invertebrates. New York: McGraw-Hill. 572 p.
- Hyman LH (1955) The invertebrates. New York: McGraw-Hill. 572 p.
Cited by
Sorted by citations
Denes, A. S., Jékely, G., Steinmetz, P. R. H., Raible, F., Snyman, H., Prud'homme, B., Ferrier, D. E. K., Balavoine, G., & Arendt, D. (2007) · Cell · doi:10.1016/j.cell.2007.02.040 · Cited by 480 · see citing works
Evo-Devo: Variations on Ancestral Themes
Robertis, E. M. D. (2008) · Cell · doi:10.1016/j.cell.2008.01.003 · Cited by 335 · see citing works
BMP gradients: A paradigm for morphogen-mediated developmental patterning
Bier, E., & Robertis, E. M. D. (2015) · Science · doi:10.1126/science.aaa5838 · Cited by 312 · see citing works
Resynthesizing behavior through phylogenetic refinement
Cisek, P. (2019) · Attention Perception & Psychophysics · doi:10.3758/s13414-019-01760-1 · Cited by 294 · see citing works
Niehrs, C. (2010) · Development · doi:10.1242/dev.039651 · Cited by 283 · 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
Axial patterning in cephalochordates and the evolution of the organizer
Yu, J., Satou, Y., Holland, N. D., Shin‐I, T., Kohara, Y., Satoh, N., Bronner-Fraser, M. E., & Holland, L. Z. (2007) · Nature · doi:10.1038/nature05472 · Cited by 256 · see citing works
Hemichordate genomes and deuterostome origins
Simakov, O., Kawashima, T., Marlétaz, F., Jenkins, J. W., Koyanagi, R., Mitros, T., Hisata, K., Bredeson, J. V., Shoguchi, E., Gyoja, F., et al. (2015) · Nature · doi:10.1038/nature16150 · Cited by 250 · see citing works
Self-citationAncient deuterostome origins of vertebrate brain signalling centres
Pani, A. M., Mullarkey, E. E., Aronowicz, J., Assimacopoulos, S., Grove, E. A., & Lowe, C. J. (2012) · Nature · doi:10.1038/nature10838 · Cited by 252 · see citing works
Self-citationDeciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives
Swalla, B. J., & Smith, A. B. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2246 · Cited by 252 · see citing works
Scaling of the BMP activation gradient in Xenopus embryos
Ben‐Zvi, D., Shilo, B., Fainsod, A., & Barkai, N. (2008) · Nature · doi:10.1038/nature07059 · Cited by 231 · see citing works
On 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
Newman, S. A., & Bhat, R. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.072481sn · Cited by 208 · 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
The evolution of nervous system centralization
Arendt, D., Denes, A. S., Jékely, G., & Tessmar-Raible, K. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2242 · Cited by 206 · see citing works
Spemann’s organizer and the self-regulation of embryonic fields
Robertis, E. M. D. (2009) · Mechanisms of Development · doi:10.1016/j.mod.2009.08.004 · Cited by 206 · see citing works
Lapraz, F., Besnardeau, L., & Lepage, T. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000248 · Cited by 202 · see citing works
Convergent evolution of bilaterian nerve cords
Martín-Durán, J. M., Pang, K., Børve, A., Semmler, H., Furu, A., Cannon, J. T., Jondelius, U., & Hejnol, A. (2017) · Nature · doi:10.1038/nature25030 · Cited by 190 · see citing works
Evolutionary crossroads in developmental biology: sea urchins
McClay, D. (2011) · Development · doi:10.1242/dev.048967 · Cited by 190 · see citing works
Evolution of bilaterian central nervous systems: a single origin?
Holland, L. Z., Carvalho, J. E., Escrivá, H., Laudet, V., Schubert, M., Shimeld, S. M., & Yu, J. (2013) · EvoDevo · doi:10.1186/2041-9139-4-27 · Cited by 186 · see citing works
The evolution of associative learning: A factor in the Cambrian explosion
Ginsburg, S., & Jablonka, E. (2010) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2010.06.017 · Cited by 184 · see citing works
Acoel development indicates the independent evolution of the bilaterian mouth and anus
Hejnol, A., & Martindale, M. Q. (2008) · Nature · doi:10.1038/nature07309 · Cited by 179 · see citing works
Li, H., Lu, Y., Smith, H., & Richardson, W. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4456-07.2007 · Cited by 180 · see citing works
Wanninger, A., & Wollesen, T. (2018) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12439 · Cited by 175 · see citing works
Chordate evolution and the three-phylum system
Satoh, N., Rokhsar, D. S., & Nishikawa, T. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.1729 · Cited by 170 · see citing works
Molina, M. D., Saló, E., & Cebrià, F. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.08.019 · Cited by 163 · see citing works
The Evolution of Early Neurogenesis
Hartenstein, V., & Stollewerk, A. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.02.004 · Cited by 161 · see citing works
The deuterostome context of chordate origins
Lowe, C. J., Clarke, D. N., Medeiros, D. M., Rokhsar, D. S., & Gerhart, J. C. (2015) · Nature · doi:10.1038/nature14434 · Cited by 155 · see citing works
Self-citationSaudemont, A., Haillot, E., Mekpoh, F., Bessodes, N., Quirin, M., Lapraz, F., Duboc, V., Röttinger, É., Range, R., Oisel, A., et al. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001259 · Cited by 148 · see citing works
Gut-like ectodermal tissue in a sea anemone challenges germ layer homology
Steinmetz, P. R. H., Aman, A. J., Kraus, J. E. M., & Technau, U. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0285-5 · Cited by 135 · see citing works
BMPs 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
Ancestral Notch-mediated segmentation revealed in the cockroach Periplaneta americana
Pueyo, J. I., Lanfear, R., & Couso, J. P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804093105 · Cited by 136 · see citing works
A 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
Tassy, O., Dauga, D., Daian, F., Sobral, D., Robin, F., Khoueiry, P., Salgado, D., Fox, V., Caillol, D., Schiappa, R., et al. (2010) · Genome Research · doi:10.1101/gr.108175.110 · Cited by 128 · see citing works
Cellular Hypoxia Promotes Heterotopic Ossification by Amplifying BMP Signaling
Wang, H., Lindborg, C. M., Lounev, V. Y., Kim, J., McCarrick-Walmsley, R., Xu, M., Mangiavini, L., Groppe, J. C., Shore, E. M., Schipani, E., et al. (2016) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2848 · Cited by 125 · see citing works
Albuixech-Crespo, B., López-Blanch, L., Burguera, D., Maeso, I., Sánchez‐Arrones, L., Moreno‐Bravo, J. A., Somorjai, I., Pascual‐Anaya, J., Puelles, E., Bovolenta, P., et al. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2001573 · Cited by 124 · see citing works
Centralization of the Deuterostome Nervous System Predates Chordates
Nomaksteinsky, M., Röttinger, É., Dufour, H. D., Chettouh, Z., Lowe, C. J., Martindale, M. Q., & Brunet, J. (2009) · Current Biology · doi:10.1016/j.cub.2009.05.063 · Cited by 121 · see citing works
Self-citationOn 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
Building a bridal chamber: development of the thalamus
Scholpp, S., & Lumsden, A. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.05.003 · Cited by 118 · see citing works
Man is but a worm: Chordate origins
Brown, F. D., Prendergast, A. E., & Swalla, B. J. (2008) · genesis · doi:10.1002/dvg.20471 · 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
The evolution of nervous system patterning: insights from sea urchin development
Angerer, L. M., Yaguchi, S., Angerer, R. C., & Burke, R. D. (2011) · Development · doi:10.1242/dev.058172 · Cited by 117 · see citing works
Chordate roots of the vertebrate nervous system: expanding the molecular toolkit
Holland, L. Z. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2703 · Cited by 114 · see citing works
Deuterostomes in a twist: the origins of a radical new body plan
Smith, A. B. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00260.x · 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
Embryology of a planktonic tunicate reveals traces of sessility
Stach, T., Winter, J., Bouquet, J., Chourrout, D. M., & Schnabel, R. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710196105 · Cited by 108 · see citing works
Evolution of behavioural control from chordates to primates
Cisek, P. (2022) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2020.0522 · Cited by 107 · see citing works
Darras, S., Gerhart, J. C., Terasaki, M., Kirschner, M. W., & Lowe, C. J. (2011) · Development · doi:10.1242/dev.059493 · Cited by 106 · see citing works
Self-citationGaviño, M. A., & Reddien, P. W. (2011) · Current Biology · doi:10.1016/j.cub.2011.01.017 · Cited by 104 · see citing works
Neural induction and early patterning in vertebrates
Ozair, M. Z., Kintner, C. R., & Brivanlou, A. H. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.90 · Cited by 99 · see citing works
Modeling Planarian Regeneration: A Primer for Reverse-Engineering the Worm
Lobo, D., Beane, W. S., & Levin, M. G. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002481 · Cited by 99 · 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
Onai, T., Yu, J., Blitz, I. L., Cho, K. W. Y., & Holland, L. Z. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.05.016 · Cited by 91 · see citing works
The Fox/Forkhead transcription factor family of the hemichordate Saccoglossus kowalevskii
Fritzenwanker, J. H., Gerhart, J. C., Freeman, R. M., & Lowe, C. J. (2014) · EvoDevo · doi:10.1186/2041-9139-5-17 · Cited by 89 · see citing works
Self-citationSelf-Regulatory Circuits in Dorsoventral Axis Formation of the Short-Germ Beetle Tribolium castaneum
da Fonseca, R. N., von Levetzow, C., Kalscheuer, P., Basal, A., van der Zee, M., & Roth, S. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.02.011 · Cited by 88 · see citing works
Molecular phylogeny of hemichordata, with updated status of deep-sea enteropneusts
Cannon, J. T., Rychel, A. L., Eccleston, H., Halanych, K. M., & Swalla, B. J. (2009) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2009.03.027 · Cited by 87 · see citing works
Lowe, C. J. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2247 · Cited by 85 · see citing works
Self-citationVergara, H. M., Bertucci, P. Y., Hantz, P., Tosches, M. A., Achim, K., Vopálenský, P., & Arendt, D. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610602114 · Cited by 84 · see citing works
Neural induction requires continued suppression of both Smad1 and Smad2 signals during gastrulation
Chang, C., & Harland, R. M. (2007) · Development · doi:10.1242/dev.007179 · Cited by 82 · see citing works
Satoh, N., Tagawa, K., & Takahashi, H. (2012) · Evolution & Development · doi:10.1111/j.1525-142x.2011.00522.x · Cited by 82 · see citing works
Integrating positional information at the level of Smad1/5/8
Eivers, E., Fuentealba, L. C., & Robertis, E. M. D. (2008) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2008.06.001 · Cited by 81 · see citing works
Uncoupling of complex regulatory patterning during evolution of larval development in echinoderms
Yankura, K. A., Martik, M. L., Jennings, C. K., & Hinman, V. F. (2010) · BMC Biology · doi:10.1186/1741-7007-8-143 · Cited by 81 · see citing works
Kin, K., Kakoi, S., & Wada, H. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.01.021 · Cited by 80 · 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
Saudemont, A., Dray, N., Hudry, B., Gouar, M. L., Vervoort, M., & Balavoine, G. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.02.013 · Cited by 78 · see citing works
Wang, W., Razy‐Krajka, F., Siu, E., Ketcham, A., & Christiaen, L. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001725 · Cited by 78 · see citing works
Harzsch, S., & Müller, C. H. G. (2007) · Frontiers in Zoology · doi:10.1186/1742-9994-4-14 · Cited by 78 · see citing works
Evolution of the bilaterian mouth and anus
Nielsen, C., Brunet, T., & Arendt, D. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0641-0 · Cited by 70 · see citing works
Kozmiková, I., Candiani, S., Fábián, P., Gurská, D., & Kozmík, Z. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.07.021 · Cited by 77 · see citing works
The evolutionary history of vertebrate cranial placodes II. Evolution of ectodermal patterning
Schlosser, G., Patthey, C., & Shimeld, S. M. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.01.019 · Cited by 74 · see citing works
Künnapuu, J., Björkgren, I., & Shimmi, O. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809885106 · Cited by 76 · see citing works
Lu, T.-M., Luo, Y., & Yu, J. (2012) · Development · doi:10.1242/dev.073833 · Cited by 75 · see citing works
Anteroposterior axis patterning by early canonical Wnt signaling during hemichordate development
Darras, S., Fritzenwanker, J. H., Uhlinger, K. R., Farrelly, E. R., Pani, A. M., Hurley, I. A., Norris, R. P., Osovitz, M., Terasaki, M., Wu, M., et al. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2003698 · Cited by 75 · see citing works
Self-citationEvolutionary crossroads in developmental biology: hemichordates
Röttinger, É., & Lowe, C. J. (2012) · Development · doi:10.1242/dev.066712 · Cited by 75 · see citing works
Self-citationAnimal regeneration: ancestral character or evolutionary novelty?
Slack, J. M. W. (2017) · EMBO Reports · doi:10.15252/embr.201643795 · Cited by 75 · see citing works
Diversification of acorn worms (Hemichordata, Enteropneusta) revealed in the deep sea
Osborn, K. J., Kuhnz, L. A., Priede, I. G., Urata, M., Gebruk, A. V., & Holland, N. D. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2011.1916 · Cited by 74 · see citing works
A developmental perspective on the evolution of the nervous system
Martín-Durán, J. M., & Hejnol, A. (2019) · Developmental Biology · doi:10.1016/j.ydbio.2019.10.003 · Cited by 72 · see citing works
Stem Cells in Marine Organisms
Rinkevich, B., & Matranga, V. (2009) · Springer eBooks · doi:10.1007/978-90-481-2767-2 · Cited by 72 · see citing works
Evolutionary crossroads in developmental biology
Patel, N. H. (2012) · Development · doi:10.1242/dev.085464 · Cited by 74 · see citing works
Molecular evidence of anteroposterior patterning in adult echinoderms
Formery, L., Peluso, P. S., Kohnle, I., Malnick, J., Thompson, J. R., Pitel, M. O., Uhlinger, K. R., Rokhsar, D. S., Rank, D. R., & Lowe, C. J. (2023) · Nature · doi:10.1038/s41586-023-06669-2 · Cited by 67 · see citing works
Self-citationEmbryonic neurogenesis in echinoderms
Hinman, V. F., & Burke, R. D. (2018) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.316 · Cited by 65 · see citing works
Cis-regulatory architecture of a brain-signaling center predates the origin of chordates
Yao, Y., Minor, P. J., Zhao, Y.-T., Jeong, Y., Pani, A. M., King, A. N., Symmons, O., Gan, L., Cardoso, W., Spitz, F., et al. (2016) · Nature Genetics · doi:10.1038/ng.3542 · Cited by 57 · see citing works
Self-citationOn the Origin and Evolution of the Tripartite Brain
Hirth, F. (2010) · Brain Behavior and Evolution · doi:10.1159/000320218 · Cited by 64 · see citing works
Ontogeny of the collar cord: Neurulation in the hemichordateSaccoglossus kowalevskii
Kaul, S., & Stach, T. (2010) · Journal of Morphology · doi:10.1002/jmor.10868 · Cited by 63 · see citing works
Perry, K. J., Lyons, D. C., Truchado-García, M., Fischer, A., Helfrich, L. W., Johansson, K. B., Diamond, J. C., Grande, C., & Henry, J. J. (2015) · Developmental Dynamics · doi:10.1002/dvdy.24308 · Cited by 63 · see citing works
Development of the enteropneust <i>Ptychodera flava</i>: Ciliary bands and nervous system
Nielsen, C., & Hay‐Schmidt, A. (2007) · Journal of Morphology · doi:10.1002/jmor.10533 · Cited by 61 · see citing works
Hemichordate neurulation and the origin of the neural tube
Miyamoto, N., & Wada, H. (2013) · Nature Communications · doi:10.1038/ncomms3713 · Cited by 61 · see citing works
Basic features of the ancestral chordate brain: A protochordate perspective
Lacalli, T. C. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.10.038 · Cited by 61 · see citing works
Irimia, M., Piñeiro, C., Maeso, I., Gómez-Skármeta, J. L., Casares, F., & García‐Fernàndez, J. (2010) · EvoDevo · doi:10.1186/2041-9139-1-7 · Cited by 61 · see citing works
A deuterostome origin of the Spemann organiser suggested by Nodal and ADMPs functions in Echinoderms
Lapraz, F., Haillot, E., & Lepage, T. (2015) · Nature Communications · doi:10.1038/ncomms9434 · Cited by 61 · see citing works
Evolution of the CNS myelin gene regulatory program
Li, H., & Richardson, W. (2015) · Brain Research · doi:10.1016/j.brainres.2015.10.013 · Cited by 53 · see citing works
TGFβ signaling in Tribolium: vertebrate-like components in a beetle
van der Zee, M., da Fonseca, R. N., & Roth, S. (2008) · Development Genes and Evolution · doi:10.1007/s00427-007-0179-7 · Cited by 58 · see citing works
Veeman, M. T., Newman-Smith, E. D., El‐Nachef, D., & Smith, W. C. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.04.028 · Cited by 58 · see citing works
FGF signaling induces mesoderm in the hemichordate Saccoglossus kowalevskii
Green, S. A., Norris, R. P., Terasaki, M., & Lowe, C. J. (2013) · Development · doi:10.1242/dev.083790 · Cited by 57 · see citing works
Self-citationThe embryonic epicardium: an essential element of cardiac development
Carmona, R., Guadix, J. A., Cano, E., Ruiz‐Villalba, A., Portillo-Sánchez, V., Pérez-Pomares, J. M., & Muñoz‐Chápuli, R. (2010) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2010.01088.x · Cited by 57 · see citing works
Horton, A. C., Mahadevan, N. R., Minguillón, C., Osoegawa, K., Rokhsar, D. S., Ruvinsky, I., de Jong, P. J., Logan, M. P. O., & Gibson‐Brown, J. J. (2008) · Development Genes and Evolution · doi:10.1007/s00427-008-0249-5 · Cited by 55 · see citing works
The Nodal signaling pathway controls left-right asymmetric development in amphioxus
Soukup, V., Yong, L. W., Lu, T.-M., Huang, S.-W., Kozmík, Z., & Yu, J. (2015) · EvoDevo · doi:10.1186/2041-9139-6-5 · Cited by 54 · see citing works
Achatz, J. G., & Martı́nez, P. (2012) · Frontiers in Zoology · doi:10.1186/1742-9994-9-27 · Cited by 53 · see citing works
Mashanov, V. S., Zueva, O. R., Heinzeller, T., Aschauer, B., Naumann, W. W., Grondona, J. M., Cifuentes, M., & García‐Arrarás, J. E. (2009) · Frontiers in Zoology · doi:10.1186/1742-9994-6-11 · Cited by 53 · see citing works
- Authors
- Lowe, C. J., Terasaki, M., Wu, M., Freeman, R. M., Runft, L., Kwan, K., Haigo, S., Aronowicz, J., Lander, E., Gruber, C., Smith, M., Kirschner, M., & Gerhart, J.
- Affiliations
- University of Chicago (US)
- UConn Health (US)
- University of California, Berkeley (US)
- Harvard University (US)
- University of California, Santa Barbara (US)
- Broad Institute (US)
- Corresponding author
- Gerhart, John
- ORCID
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2006-08-22
- Volume
- 4
- Issue
- 9
- Pages
- e291
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- OpenAlex
- W2129829180
- Cited by
- 385
- References
- 102
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 23 · 2023: 10 · 2022: 10 · 2021: 11 · 2020: 18 · 2019: 12 · 2018: 15 · 2017: 20 · 2016: 14 · 2015: 29 · 2014: 16 · 2013: 14 · 2012: 16
- FWCI
- 17.42
- Type
- journal article
- Language
- en
- Update notices
- correction (2015-12-29)
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Knowledge@UChicago (University of Chicago) (submittedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- University of Chicago (cc-by)
- Funders
- National Aeronautics and Space Administration
- Adolph C. and Mary Sprague Miller Institute for Basic Research in Science, University of California Berkeley
- U.S. Public Health Service
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD 42724, R01HD042724, HD37277, R01HD037277, T32HD007491)
- 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
- dorsoventral patterning, hemichordates, chordate evolution, bone morphogenetic proteins, chordin, germ layer patterning, ventralization, mouth position
- MeSH terms
- Animals, Chordata, Nonvertebrate, Biological Evolution, Glycoproteins, Gene Expression Regulation, Developmental, Bone Morphogenetic Proteins, Body Patterning, Intercellular Signaling Peptides and Proteins
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
