Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning
Open accessAbstract
The conservation of developmental functions exerted by Antp-class homeoproteins in protostomes and deuterostomes suggested that homologs with related functions are present in diploblastic animals. Our phylogenetic analyses showed that Antp-class homeodomains belong either to non-Hox or to Hox/paraHox families. Among the 13 non-Hox families, 9 have diploblastic homologs, Msx, Emx, Barx, Evx, Tlx, NK-2, and Prh/Hex, Not, and Dlx, reported here. Among the Hox/paraHox, poriferan sequences were not found, and the cnidarian sequences formed at least five distinct cnox families. Two are significantly related to the paraHox Gsx (cnox-2) and the mox (cnox-5) sequences, whereas three display some relatedness to the Hox paralog groups 1 (cnox-1), 9/10 (cnox-3) and the paraHox cdx (cnox-4). Intermediate Hox/paraHox genes (PG 3 to 8 and lox) did not have clear cnidarian counterparts. In Hydra, cnox-1, cnox-2, and cnox-3 were not found chromosomally linked within a 150-kb range and displayed specific expression patterns in the adult head. During regeneration, cnox-1 was expressed as an early gene whatever the polarity, whereas cnox-2 was up-regulated later during head but not foot regeneration. Finally, cnox-3 expression was reestablished in the adult head once it was fully formed. These results suggest that the Hydra genes related to anterior Hox/paraHox genes are involved at different stages of apical differentiation. However, the positional information defining the oral/aboral axis in Hydra cannot be correlated strictly to that characterizing the anterior-posterior axis in vertebrates or arthropods.
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?
The Cnox4-Pc homeodomain carries diagnostic amino acids K4, R10, and D29, indicating some relatedness to posterior Hox genes of PG-9,10.
“The Cnox4-Pc homeodomain carries those diagnostic amino acids (K4, R10, D29), therefore it has some relatedness with the”
From Conservation of Hox/ParaHox-Related Genes in the Early Development of a Cnidarian (2001) · cites this paper as Gauchat et al., 2000
One group of Cnox-3 class genes shares specific amino acids with the bilaterian PG-9,10 homeodomain.
“As pointed out by Gauchat et al. (2000), one group of the Cnox-3 class genes shares specific amino acids with the homeodomain of the bilaterian PG-9,10.”
From Conservation of Hox/ParaHox-Related Genes in the Early Development of a Cnidarian (2001) · cites this paper as Gauchat et al., 2000
Similarities in the homeodomain and N terminus of Gsx with bilaterian sequences confirm that ParaHox genes are present in cnidarians.
“In the case of Gsx, similarities inside the homeodomain and at the N terminus of the protein (not shown) with corresponding sequences from bilaterians confirm once more that ParaHox genes are present in cnidarians (Gauchat et al., 2000;Kourakis and Martindale, 2000).”
From Conservation of Hox/ParaHox-Related Genes in the Early Development of a Cnidarian (2001) · cites this paper as Gauchat et al., 2000
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
Molecular Cloning: A Laboratory Manual
Sambrook, J., Fritsch, E., & Maniatis, T. (1989) · UCLA - Biblioteca de Ciencias de la Salud · Cited by 133,589 · see citing works
Molecular cloning: A laboratory manual
Deininger, P. L. (1990) · Analytical Biochemistry · doi:10.1016/0003-2697(90)90595-z · Cited by 84,684 · see citing works
The neighbor-joining method: a new method for reconstructing phylogenetic trees.
Saitou, N., & Nei, M. (1987) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040454 · Cited by 59,962 · see citing works
Atlas of protein sequence and structure
Chang, M.-Y., Dayhoff, M. O., Eck, R. V., & Sochard, M. R. (1965) · NASA Technical Reports Server (NASA) · Cited by 4,383 · see citing works
A gene complex controlling segmentation in Drosophila
Lewis, E. B. (1978) · Nature · doi:10.1038/276565a0 · Cited by 3,813 · see citing works
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
Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies
Strimmer, K., & von Haeseler, A. (1996) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025664 · Cited by 2,531 · see citing works
Atlas of Protein Sequence and Structure, 1972.
Fitch, W. M., & Dayhoff, M. O. (1973) · Systematic Zoology · doi:10.2307/2412105 · Cited by 2,458 · see citing works
SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny
Galtier, N., Gouy, M., & Gautier, C. (1996) · Computer applications in the biosciences · doi:10.1093/bioinformatics/12.6.543 · Cited by 2,264 · see citing works
PHYLOGENIES FROM MOLECULAR SEQUENCES: INFERENCE AND RELIABILITY
Felsenstein, J. (1988) · Annual Review of Genetics · doi:10.1146/annurev.ge.22.120188.002513 · Cited by 2,159 · see citing works
The ribosomal database project
Larsen, N., Olsen, G. J., Maidak, B. L., McCaughey, M. J., Overbeek, R., Macke, T. J., Marsh, T. L., & Woese, C. R. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.13.3021 · Cited by 1,558 · see citing works
Graham, A., Papalopulu, N., & Krumlauf, R. K. (1989) · Cell · doi:10.1016/0092-8674(89)90912-4 · Cited by 1,004 · see citing works
Duboule, D., & Dollé, P. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb03534.x · Cited by 941 · see citing works
Nested expression domains of four homeobox genes in developing rostral brain
Simeone, A., Acampora, D., Gulisano, M., Stornaiuolo, A., & Boncinelli, E. (1992) · Nature · doi:10.1038/358687a0 · Cited by 793 · see citing works
The zootype and the phylotypic stage
Slack, J. M. W., Holland, P. W. H., & Graham, C. F. (1993) · Nature · doi:10.1038/361490a0 · Cited by 699 · see citing works
Hox genes in brachiopods and priapulids and protostome evolution
de Rosa, R., Grenier, J. K., Andreeva, T., Cook, C. E., Adoutte, A., Akam, M., Carroll, S. B., & Balavoine, G. (1999) · Nature · doi:10.1038/21631 · Cited by 541 · 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
Whole-mount in situ hybridization in the mouse embryo: gene expression in three dimensions
Rosen, B. P., & Beddington, R. S. P. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90162-b · Cited by 205 · see citing works
Hydra transplantation phenomena and the mechanism of Hydra head regeneration
MacWilliams, H. K. (1983) · Developmental Biology · doi:10.1016/0012-1606(83)90325-1 · Cited by 197 · see citing works
CnNK-2,an NK-2 Homeobox Gene, Has a Role in Patterning the Basal End of the Axis in Hydra
Grens, A., Gee, L., Fisher, D. A., & Bode, H. R. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0321 · Cited by 192 · see citing works
A comprehensive classification of homeobox genes
Bürglin, T. R. (1994) · doi:10.1093/oso/9780198599395.003.0003 · Cited by 189 · see citing works
Evolution of homeobox genes: Q50 Paired-like genes founded the Paired class
Galliot, B., de Vargas, C., & Miller, D. J. (1999) · Development Genes and Evolution · doi:10.1007/s004270050243 · Cited by 188 · see citing works
Self-citationSchummer, M., Scheurlen, I., Schaller, C., & Galliot, B. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05233.x · Cited by 174 · see citing works
Self-citationThe homeo box: A key to the understanding of development?
Gehring, W. J. (1985) · Cell · doi:10.1016/0092-8674(85)90300-9 · Cited by 173 · see citing works
Detection of homeobox genes in development and evolution.
Murtha, M. T., Leckman, J. F., & Ruddle, F. H. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.23.10711 · Cited by 168 · 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
Evolution of Antennapedia-Class Homeobox Genes
Zhang, J., & Nei, M. (1996) · Genetics · doi:10.1093/genetics/142.1.295 · Cited by 137 · see citing works
Hox genes in evolution: protein surfaces and paralog groups
Sharkey, M. (1997) · Trends in Genetics · doi:10.1016/s0168-9525(97)01096-2 · Cited by 131 · 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
Schubert, F. R., Nieselt-Struwe, K., & Gruss, P. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.1.143 · Cited by 119 · see citing works
Homology of Hox Genes and the Zootype Concept in Early Metazoan Evolution
Schierwater, B., & Kuhn, K. (1998) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.1998.0489 · Cited by 98 · see citing works
Homeobox‐containing genes in the most primitive metazoa, the sponges
Seimiya, M., ISHIGURO, H., Miura, K., WATANABE, Y., & Kurosawa, Y. (1994) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1994.tb18732.x · Cited by 96 · see citing works
A hox/hom homeobox gene in sponges
Degnan, B. M., Degnan, B. M., Giusti, A. F., & Morse, D. E. (1995) · Gene · doi:10.1016/0378-1119(94)00908-b · Cited by 79 · see citing works
Schierwater, B., Murtha, M. T., Dick, M. H., Ruddle, F. H., & Buss, L. W. (1991) · Journal of Experimental Zoology · doi:10.1002/jez.1402600316 · Cited by 75 · 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
Finnerty, J. R., & Martindale, M. Q. (1997) · Biological Bulletin · doi:10.2307/1542736 · 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
Gauchat, D., Kreger, S., Holstein, T. W., & Galliot, B. (1998) · Development · doi:10.1242/dev.125.9.1637 · Cited by 66 · see citing works
Self-citationGalliot, B., & Miller, D. J. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(99)01888-0 · Cited by 65 · see citing works
Self-citationExpression of a Hox gene, Cnox-2, and the division of labor in a colonial hydroid
Cartwright, P., Bowsher, J. H., & Buss, L. W. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.5.2183 · Cited by 63 · see citing works
Expression of Cnox-2, a HOM/HOX Gene, Is Suppressed during Head Formation in Hydra
Shenk, M. A., Gee, L., Steele, R. E., & Bode, H. R. (1993) · Developmental Biology · doi:10.1006/dbio.1993.1290 · Cited by 61 · see citing works
Balavoine, G., & Telford, M. J. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.16.7227 · Cited by 59 · 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
Aerne, B. L., Baader, C. D., & Schmid, V. J. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1168 · Cited by 54 · see citing works
Mokady, O., Dick, M. H., Lackschewitz, D., Schierwater, B., & Buss, L. W. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.7.3673 · Cited by 53 · see citing works
Dollé, P., Fraulob, V., & Duboule, D. (1994) · Development · doi:10.1242/dev.1994.supplement.143 · Cited by 51 · see citing works
Presence of eight distinct homeobox‐containing genes in cnidarians
Naito, M., Ishiguro, H., Fujisawa, T., & Kurosawa, Y. (1993) · FEBS Letters · doi:10.1016/0014-5793(93)80668-k · Cited by 44 · see citing works
Miles, A., & Miller, D. J. (1992) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1992.0057 · Cited by 36 · see citing works
Size and stability of the genomes of the myxobacteria Stigmatella aurantiaca and Stigmatella erecta
Neumann, B., Pospiech, A., & Schairer, H. U. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.19.6307-6310.1992 · Cited by 30 · see citing works
A quantitative method for separation of livingHydra cells
Greber, M. J., David, C. N., & Holstein, T. W. (1992) · Development Genes and Evolution · doi:10.1007/bf00592110 · Cited by 26 · 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
Richelle-Maurer, E., & Vyver, G. V. D. (1999) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(99)00037-8 · Cited by 23 · see citing works
‘Guessmer’ screening strategy applied to species with AT-rich coding sequences
Galliot, B., & Schummer, M. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90051-i · Cited by 10 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 3
- [32]Bürglin T R. In: Guide to the Homeobox Genes. Duboule D, editor. New York: Oxford Univ. Press; 1994. pp. 27–71. [Google Scholar]
- [40]Strimmer K, von Haeseler A. Mol Biol Evol. 1996;13:964–969. [Google Scholar]
- [47]Dolle P, Fraulob V, Duboule D. Development (Cambridge, U.K.) 1994. Suppl., 143–153. [PubMed] [Google Scholar]
Cited by
Sorted by citations
WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra
Hobmayer, B., Rentzsch, F., Kuhn, K., Happel, C. M., von Laue, C. C., Snyder, P., Rothbächer, U., & Holstein, T. W. (2000) · Nature · doi:10.1038/35025063 · Cited by 599 · see citing works
Peterson, K. J., & Eernisse, D. J. (2001) · Evolution & Development · doi:10.1046/j.1525-142x.2001.003003170.x · Cited by 529 · 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
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
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
Self-citationA 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
Gene structure and larval expression of cnox-2Am from the coral Acropora millepora
C. Hayward, D., Catmull, J., Reece-Hoyes, J. S., Berghammer, H., Dodd, H., Hann, S. J., Miller, D. J., & Ball, E. E. (2001) · Development Genes and Evolution · doi:10.1007/s004270000112 · Cited by 79 · see citing works
The Role of Hox Genes in Axial Patterning in Hydra1
Bode, H. R. (2001) · American Zoologist · doi:10.1668/0003-1569(2001)041[0621:trohgi]2.0.co;2 · Cited by 18 · see citing works
- Authors
- Gauchat, D., Mazet, F., Berney, C., Schummer, M., Kreger, S., Pawlowski, J., & Galliot, B.
- Affiliations
- University of Geneva (CH)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2000-04-25
- Volume
- 97
- Issue
- 9
- Pages
- 4493-4498
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC18262
- OpenAlex
- W2090110356
- Cited by
- 190
- References
- 53
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 3 · 2022: 2 · 2020: 5 · 2019: 5 · 2018: 2 · 2017: 3 · 2016: 5 · 2015: 5 · 2014: 1 · 2013: 1 · 2012: 10
- FWCI
- 5.66
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- 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 › Genomics and Chromatin Dynamics
- Keywords
- Hydra, anterior patterning, head regeneration, oral-aboral axis, anterior-posterior axis, gene expression patterns
- MeSH terms
- Amino Acid Sequence, Animals, Cloning, Molecular, Genes, Homeobox, Multigene Family, Hydra, Molecular Sequence Data, Nuclear Proteins, Phylogeny, Transcription Factors, Electrophoresis, Gel, Pulsed-Field, Conserved Sequence, Homeodomain Proteins, Evolution, Molecular, Body Patterning, Antennapedia Homeodomain Protein
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
