Zebrafish hox Clusters and Vertebrate Genome Evolution
Abstract
HOX genes specify cell fate in the anterior-posterior axis of animal embryos. Invertebrate chordates have one HOXcluster, but mammals have four, suggesting that cluster duplication facilitated the evolution of vertebrate body plans. This report shows that zebrafish have seven hox clusters. Phylogenetic analysis and genetic mapping suggest a chromosome doubling event, probably by whole genome duplication, after the divergence of ray-finned and lobe-finned fishes but before the teleost radiation. Thus, teleosts, the most species-rich group of vertebrates, appear to have more copies of these developmental regulatory genes than do mammals, despite less complexity in the anterior-posterior axis.
Get full access to this article
View all available purchase options and get full access to this article.
Supplementary Material
File (983268.xhtml)
- Download
- 216.26 KB
REFERENCES AND NOTES
1
Krumlauf R., Cell 78, 191 (1994);
Kmita-Cunisse M., Loosli F., Bierne J., Gehring W., Proc. Natl. Acad. Sci. U.S.A. 95, 3030 (1998);
Kourakis M., et al., Dev. Biol. 190, 284 (1997);
Lewis E. B., Nature 276, 565 (1978);
Dickman S., Science 275, 1568 (1997).
2
Duboule D., Dollé P., EMBO J. 8, 1497 (1989).
3
Garcia-Fernandez J., Holland P. W. H., Nature 370, 563 (1994);
Di Gregorio A., et al., Gene 156, 253 (1995).
4
Holland P. W. H., Garcia-Fernandez J., Dev. Biol. 173, 382 (1996);
Sharman A., Holland P. W. H., Neth. J. Zool. 46, 47 (1996).
5
Aparicio S., et al., Nature Genet. 16, 79 (1997).
6
Misof B., Wagner G., Mol. Phylogenet. Evol. 5, 309 (1996).
7
van der Hoeven F., Sordino P., Fraudeau N., Izpisua-Belmonte J. C., Duboule D., Mech. Dev. 54, 9 (1996);
Misof B., Blanco M., Wagner G., J. Exp. Zool. 274, 193 (1996) ;
Prince V., Joly L., Ekker M., Ho R., Development 125, 407 (1998).
8
Eiken H. G., Njolstad P. R., Molven A., Fjose A., Biochem. Biophys. Res. Commun. 149, 1165 (1987);
Njolstad P., Molven A., Hordvik I., Apold J., Fjose A., Nucleic Acids Res. 16, 9097 (1988) ;
Njolstad P. R., Molven A., Eiken H. G., Fjose A., Gene 73, 33 (1989);
Njolstad P. R., Molven A., Apold J., Fjose A., EMBO J. 9, 515 (1990) ;
Runstadler J. A., Kocher T. D., Nucleic Acids Res. 19, 5434 (1991);
Sordino P., Duboule D., Kondo T., Mech. Dev. 59, 165 (1996);
Prince V., Moens C., Kimmel C., Ho R., Development 125, 393 (1997).
9
DNA pools (plate pools, then row and column pools) from an arrayed zebrafish PAC library (19) were screened with redundant primers (Hox-F: 5′-CGNAAGAARMGNGTNCCNTAYAC-3′; Hox-R: 5′-CATNCKNCKRTTYTGRAACCANAT-3′; Hox-Fi: 5′-CTNGARYTNGARAARGARTTYCA), where N is A, C, T, or G, R is A or G, M is A or C, Y is C or T, and K is T or G. Ends of positive PACs were sequenced and specific primers used to find overlapping clones. Positive PACs were amplified with redundant primers; products were cloned and sequenced, and gene specific primers were used to obtain sequence directly from PAC DNA.
10
Unambiguously alignable sequences were obtained using CLUSTAL X and trees were generated by the neighbor-joining method [
Saitou N., Nei M., Mol. Biol. Evol. 4, 406 (1987);
]. A lamprey (Petromyzon marinus) cDNA library screened with redundant hox gene primers provided an outgroup. For accession numbers, see (11).
11
See Science Online (www.sciencemag.org) for a catalog of zebrafish hox genes, alignments for the phylogenetic trees in Fig. 2, accession numbers of loci used to construct the phylogenetic trees, mapping primers for zebrafish genes, and mapping data for newly mapped loci.
12
Ahlberg P., Milner A., Nature 368, 507 (1994).
13
Zhang J., Nei M., Genetics 142, 295 (1996);
Kappen C., Ruddle F., Curr. Opin. Genet. Dev. 3, 931 (1993).
14
Bailey W., Kim J., Wagner G., Ruddle F., Mol. Biol. Evol. 14, 843 (1997);
Meyer A., Nature 391, 225 (1998).
15
Cantatore P., et al., J. Mol. Evol. 39, 589 (1994).
16
D. G. Buth, T. Dowling, J. R. Gold, in Cyprinid Fishes: Systematics, Biology, and Exploitation, I. J. Winfield and J. S. Nelson, Eds. (Chapman and Hall, London, 1991), pp. 83–126; F. W. Allendorf and G. H. Thorgaard, in Evolutionary Genetics of Fishes, J. B. Turner, Ed. (Plenum, New York, 1984), pp. 1–53.
17
Postlethwait J. H., et al., Nature Genet. 18, 345 (1998).
18
Ferris S. D., Whitt G. S., J. Mol. Evol. 12, 267 (1979);
Hughes A. L., Proc. R. Soc. London Ser. B 256, 119 (1994);
; A. Force et al., in preparation.
19
C. Amemiya, unpublished data.
20
Supported by NIH grant R01RR10715 (J.H.P.), NIH grant PHS P01HD22486 (J.H.P. and M.W.), a Medical Research Council of Canada grant (M.E.), and NSF grant IBN-9614940 (C.A.). We thank J. Miles for technical assistance.
(0)eLetters
eLetters is a forum for ongoing peer review. eLetters are not edited, proofread, or indexed, but they are screened. eLetters should provide substantive and scholarly commentary on the article. Embedded figures cannot be submitted, and we discourage the use of figures within eLetters in general. If a figure is essential, please include a link to the figure within the text of the eLetter. Please read our Terms of Service before submitting an eLetter.
Log In to Submit a ResponseNo eLetters have been published for this article yet.
Information & Authors
Information
Published In
Science
Volume 282 | Issue 5394
27 November 1998
27 November 1998
Submission history
Received: 18 June 1998
Accepted: 23 October 1998
Published in print: 27 November 1998
Authors
Metrics & Citations
Metrics
Article Usage
Altmetrics
Citations
Cite as
- Angel Amores et al.
Export citation
Select the format you want to export the citation of this publication.
Cited by
- Hox genes control homocercal caudal fin development and evolution, Science Advances, 10, 3, (2024)./doi/10.1126/sciadv.adj5991
- Bovine HOXA11 Gene Identified from RNA-Seq: mRNA Profile Analysis and Genetic Variation Detection Using ME Method and Their Associations with Carcass Traits, Cells, 12, 4, (539), (2023).https://doi.org/10.3390/cells12040539
- Genome-wide identification and characterization of toll-like receptor 5 (TLR5) in fishes, Frontiers in Genetics, 13, (2023).https://doi.org/10.3389/fgene.2022.1083578
- Hox genes in development and beyond, Development, 150, 1, (2023).https://doi.org/10.1242/dev.192476
- Hox, homology, and parsimony: An organismal perspective, Seminars in Cell & Developmental Biology, (2023).https://doi.org/10.1016/j.semcdb.2023.01.007
- Creation of intermuscular bone-free mutants in amphitriploid gibel carp by editing two duplicated runx2b homeologs, Aquaculture, 567, (739300), (2023).https://doi.org/10.1016/j.aquaculture.2023.739300
- Efficiently Editing Multiple Duplicated Homeologs and Alleles for Recurrent Polyploids, Polyploidy, (491-512), (2023).https://doi.org/10.1007/978-1-0716-2561-3_26
- Sex Lethal Gene Manipulates Gonadal Development of Medaka, Oryzias latipes, through Estrogenic Interventions, International Journal of Molecular Sciences, 23, 24, (15496), (2022).https://doi.org/10.3390/ijms232415496
- HOX-Gene Cluster Organization and Genome Duplications in Fishes and Mammals: Transcript Variant Distribution along the Anterior–Posterior Axis, International Journal of Molecular Sciences, 23, 17, (9990), (2022).https://doi.org/10.3390/ijms23179990
- Paralogous Genes Involved in Embryonic Development: Lessons from the Eye and other Tissues, Genes, 13, 11, (2082), (2022).https://doi.org/10.3390/genes13112082
- See more
Loading...
View Options
Check Access
Log in to view the full text
AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.
- Become a AAAS Member
- Activate your AAAS ID
- Purchase Access to Other Journals in the Science Family
- Account Help
Log in via OpenAthens.
Log in via Shibboleth.
More options
Register for free to read this article
As a service to the community, this article is available for free. Login or register for free to read this article.
Buy a single issue of Science for just $15 USD.