Molecular evolution of the HoxA cluster in the three major gnathostome lineages
10.1073/pnas.052709899
Crossref journal-article
Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences (341)
Abstract

The duplication of Hox clusters and their maintenance in a lineage has a prominent but little understood role in chordate evolution. Here we examined how Hox cluster duplication may influence changes in cluster architecture and patterns of noncoding sequence evolution. We sequenced the entire duplicated HoxAa and HoxAb clusters of zebrafish ( Danio rerio ) and extended the 5′ (posterior) part of the HoxM (HoxA-like) cluster of horn shark ( Heterodontus francisci ) containing the hoxa11 and hoxa13 orthologs as well as intergenic and flanking noncoding sequences. The duplicated HoxA clusters in zebrafish each house considerably fewer genes and are dramatically shorter than the single HoxA clusters of human and horn shark. We compared the intergenic sequences of the HoxA clusters of human, horn shark, zebrafish (Aa, Ab), and striped bass and found extensive conservation of noncoding sequence motifs, i.e., phylogenetic footprints, between the human and horn shark, representing two of the three gnathostome lineages. These are putative cis-regulatory elements that may play a role in the regulation of the ancestral HoxA cluster. In contrast, homologous regions of the duplicated HoxAa and HoxAb clusters of zebrafish and the HoxA cluster of striped bass revealed a striking loss of conservation of these putative cis-regulatory sequences in the 3′ (anterior) segment of the cluster, where zebrafish only retains single representatives of group 1, 3, 4, and 5 (HoxAa) and group 2 (HoxAb) genes and in the 5′ part of the clusters, where zebrafish retains two copies of the group 13, 11, and 9 genes, i.e., AbdB-like genes. In analyzing patterns of cis-sequence evolution in the 5′ part of the clusters, we explicitly looked for evidence of complementary loss of conserved noncoding sequences, as predicted by the duplication-degeneration-complementation model in which genetic redundancy after gene duplication is resolved because of the fixation of complementary degenerative mutations. Our data did not yield evidence supporting this prediction. We conclude that changes in the pattern of cis-sequence conservation after Hox cluster duplication are more consistent with being the outcome of adaptive modification rather than passive mechanisms that erode redundancy created by the duplication event. These results support the view that genome duplications may provide a mechanism whereby master control genes undergo radical modifications conducive to major alterations in body plan. Such genomic revolutions may contribute significantly to the evolutionary process.

Bibliography

Chiu, C., Amemiya, C., Dewar, K., Kim, C.-B., Ruddle, F. H., & Wagner, G. P. (2002). Molecular evolution of the HoxA cluster in the three major gnathostome lineages. Proceedings of the National Academy of Sciences, 99(8), 5492–5497.

Authors 6
  1. Chi-hua Chiu (first)
  2. Chris Amemiya (additional)
  3. Ken Dewar (additional)
  4. Chang-Bae Kim (additional)
  5. Frank H. Ruddle (additional)
  6. Günter P. Wagner (additional)
References 39 Referenced 79
  1. W McGinnis, R Krumlauf Cell 68, 283–302 (1992). (10.1016/0092-8674(92)90471-N) / Cell by McGinnis W (1992)
  2. C Kappen, K Schughart, F H Ruddle Proc Natl Acad Sci USA 86, 5459–5463 (1989). (10.1073/pnas.86.14.5459) / Proc Natl Acad Sci USA by Kappen C (1989)
  3. Akam M. Averof M. Castelli-Gair J. Dawes R. Falciani F. & Ferrier D. (1994) Dev. Suppl . 209–215. (10.1242/dev.1994.Supplement.209)
  4. B B Wang, M M Muller-Immergluck, J Austin, N T Robinson, A Chisholm, C Kenyon Cell 74, 29–42 (1993). (10.1016/0092-8674(93)90292-X) / Cell by Wang B B (1993)
  5. J Garcia-Fernandez, P W Holland Nature (London) 370, 563–566 (1994). (10.1038/370563a0) / Nature (London) by Garcia-Fernandez J (1994)
  6. P Martinez, J P Rast, C Arenas-Mena, E H Davidson Proc Natl Acad Sci USA 96, 1469–1474 (1999). (10.1073/pnas.96.4.1469) / Proc Natl Acad Sci USA by Martinez P (1999)
  7. T P Powers, J Hogan, Z Ke, K Dymbrowski, X Wang, F H Collins, T C Kaufman Evol Dev 6, 311–325 (2000). (10.1046/j.1525-142x.2000.00072.x) / Evol Dev by Powers T P (2000)
  8. M P Devenport, C Blass, P Eggleston Evol Dev 6, 326–339 (2000). (10.1046/j.1525-142x.2000.00074.x) / Evol Dev by Devenport M P (2000)
  9. R Krumlauf Cell 78, 191–201 (1994). (10.1016/0092-8674(94)90290-9) / Cell by Krumlauf R (1994)
  10. A Amores, A Force, Y Yan, L Joly, C Amemiya, A Fritz, R K Ho, J Langeland, V Prince, Y L Wang, et al. Science 282, 1711–1714 (1998). (10.1126/science.282.5394.1711) / Science by Amores A (1998)
  11. D E Ferrier, C Minguillon, P W Holland, J Garcia-Fernandez Evol Dev 5, 284–293 (2000). (10.1046/j.1525-142x.2000.00070.x) / Evol Dev by Ferrier D E (2000)
  12. E Malaga-Trillo, A Meyer Am Zool 41, 676–686 (2001). / Am Zool by Malaga-Trillo E (2001)
  13. C-B Kim, C Amemiya, W Bailey, K Kawasaki, J Mezey, W Miller, S Minoshima, N Shimizu, G Wagner, F H Ruddle Proc Natl Acad Sci USA 97, 1655–1660 (2000). (10.1073/pnas.030539697) / Proc Natl Acad Sci USA by Kim C-B (2000)
  14. S Aparicio, K Hawker, A Cottage, Y Mikawa, L Zuo, B Venkatesh, E Chen, R Krumlauf, S Brenner Nat Genet 16, 79–83 (1997). (10.1038/ng0597-79) / Nat Genet by Aparicio S (1997)
  15. E A Snell, J L Scemama, E J Stellwag J Exp Zool 285, 41–49 (1999). (10.1002/(SICI)1097-010X(19990415)285:1<41::AID-JEZ5>3.0.CO;2-D) / J Exp Zool by Snell E A (1999)
  16. C-h Chiu, D Nonaka, L Xue, C T Amemiya, G P Wagner Mol Phylogenet Evol 17, 305–316 (2000). (10.1006/mpev.2000.0837) / Mol Phylogenet Evol by Chiu C-h (2000)
  17. C-h Chiu, C T Amemiya, J L Carr, J Bhargava, J K Hwang, C S Shashikant, F H Ruddle, G P Wagner Dev Genes Evol 210, 105–109 (2000). (10.1007/s004270050016) / Dev Genes Evol by Chiu C-h (2000)
  18. S Schwartz, Z Zhang, K A Frazer, A Smit, C Riemer, J Bouck, R Gibbs, R Hardison, W Miller Genome Res 10, 577–586 (2000). (10.1101/gr.10.4.577) / Genome Res by Schwartz S (2000)
  19. D A Tagle, B F Koop, M Goodman, J L Slightom, D L Hess, R T Jones J Mol Biol 203, 439–455 (1988). (10.1016/0022-2836(88)90011-3) / J Mol Biol by Tagle D A (1988)
  20. R Hardison, J L Slightom, D L Gumucio, M Goodman, N Stojanovic, W Miller Gene 205, 73–94 (1997). (10.1016/S0378-1119(97)00474-5) / Gene by Hardison R (1997)
  21. J D Thompson, D G Higgins, T J Gibson Nucleic Acids Res 22, 4673–4680 (1994). (10.1093/nar/22.22.4673) / Nucleic Acids Res by Thompson J D (1994)
  22. J Zhu, J S Liu, C E Lawrence Bioinformatics 14, 25–39 (1998). (10.1093/bioinformatics/14.1.25) / Bioinformatics by Zhu J (1998)
  23. T J Longhurst, J M Joss J Exp Zool 285, 140–145 (1999). (10.1002/(SICI)1097-010X(19990815)285:2<140::AID-JEZ6>3.0.CO;2-V) / J Exp Zool by Longhurst T J (1999)
  24. S J Gaunt Dev Dyn 221, 26–36 (2001). (10.1002/dvdy.1122) / Dev Dyn by Gaunt S J (2001)
  25. C Larochelle, M Tremblay, D Bernier, J Aubin, L Jeannotte Dev Dyn 214, 127–140 (1999). (10.1002/(SICI)1097-0177(199902)214:2<127::AID-AJA3>3.0.CO;2-F) / Dev Dyn by Larochelle C (1999)
  26. S Nonchev, M Maconochie, C Vesque, S Aparicio, L Ariza-McNaughton, M Manzanares, K Maruthainar, A Kuroiwa, S Brenner, P Charnay, R Krumlauf Proc Natl Acad Sci USA 93, 9339–9345 (1996). (10.1073/pnas.93.18.9339) / Proc Natl Acad Sci USA by Nonchev S (1996)
  27. C S Shashikant, C-B Kim, M A Borbely, W C Wang, F H Ruddle Proc Natl Acad Sci USA 95, 15446–15451 (1998). (10.1073/pnas.95.26.15446) / Proc Natl Acad Sci USA by Shashikant C S (1998)
  28. Sumiyama K. Kim C.-B. & Ruddle F. H. (2001) 71 260–262. (10.1006/geno.2000.6422)
  29. Chiu C.-h. & Hamrick M. W. (2002) Evol. Anthropol. in press.
  30. F H Ruddle, C T Amemiya, J L Carr, C-B Kim, C Ledje, C S Shashikant, G P Wagner Ann NY Acad Sci 870, 238–248 (1999). (10.1111/j.1749-6632.1999.tb08884.x) / Ann NY Acad Sci by Ruddle F H (1999)
  31. A L Hughes Proc R Soc London Ser B 256, 119–124 (1994). (10.1098/rspb.1994.0058) / Proc R Soc London Ser B by Hughes A L (1994)
  32. A Force, M Lynch, F B Pickett, A Amores, Y L Yan, J Postlethwait Genetics 151, 1531–1545 (1999). (10.1093/genetics/151.4.1531) / Genetics by Force A (1999)
  33. K M Weiss, S M Fullerton Theor Popul Biol 57, 187–195 (2000). (10.1006/tpbi.2000.1460) / Theor Popul Biol by Weiss K M (2000)
  34. J R True, E S Haag Evol Dev 3, 109–119 (2001). (10.1046/j.1525-142x.2001.003002109.x) / Evol Dev by True J R (2001)
  35. M Z Ludwig, C Bergman, N H Patel, M Kreitman Nature (London) 403, 564–567 (2000). (10.1038/35000615) / Nature (London) by Ludwig M Z (2000)
  36. S Ohno Evolution by Gene Duplication (Springer, New York, 1970). (10.1007/978-3-642-86659-3) / Evolution by Gene Duplication by Ohno S (1970)
  37. C V Kirchhamer, C H Yuh, E H Davidson Proc Natl Acad Sci USA 93, 9322–9328 (1996). (10.1073/pnas.93.18.9322) / Proc Natl Acad Sci USA by Kirchhamer C V (1996)
  38. E T Dermitzakis, A G Clark Mol Biol Evol 18, 557–562 (2001). (10.1093/oxfordjournals.molbev.a003835) / Mol Biol Evol by Dermitzakis E T (2001)
  39. Y Van De Peer, J S Taylor, I Braasch, A Meyer J Mol Evol 53, 436–446 (2001). (10.1007/s002390010233) / J Mol Evol by Van De Peer Y (2001)
Dates
Type When
Created 23 years, 1 month ago (July 26, 2002, 10:45 a.m.)
Deposited 3 years, 2 months ago (June 7, 2022, 2:21 a.m.)
Indexed 4 months, 4 weeks ago (April 8, 2025, 10:40 p.m.)
Issued 23 years, 4 months ago (April 9, 2002)
Published 23 years, 4 months ago (April 9, 2002)
Published Online 23 years, 4 months ago (April 9, 2002)
Published Print 23 years, 4 months ago (April 16, 2002)
Funders 0

None

@article{Chiu_2002, title={Molecular evolution of the HoxA cluster in the three major gnathostome lineages}, volume={99}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.052709899}, DOI={10.1073/pnas.052709899}, number={8}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Chiu, Chi-hua and Amemiya, Chris and Dewar, Ken and Kim, Chang-Bae and Ruddle, Frank H. and Wagner, Günter P.}, year={2002}, month=apr, pages={5492–5497} }