Heterochronic shift in Hox-mediated activation of sonic hedgehog leads to morphological changes during fin development
- PMID: 19365553
- PMCID: PMC2664896
- DOI: 10.1371/journal.pone.0005121
Heterochronic shift in Hox-mediated activation of sonic hedgehog leads to morphological changes during fin development
Abstract
We explored the molecular mechanisms of morphological transformations of vertebrate paired fin/limb evolution by comparative gene expression profiling and functional analyses. In this study, we focused on the temporal differences of the onset of Sonic hedgehog (Shh) expression in paired appendages among different vertebrates. In limb buds of chick and mouse, Shh expression is activated as soon as there is a morphological bud, concomitant with Hoxd10 expression. In dogfish (Scyliorhinus canicula), however, we found that Shh was transcribed late in fin development, concomitant with Hoxd13 expression. We utilized zebrafish as a model to determine whether quantitative changes in hox expression alter the timing of shh expression in pectoral fins of zebrafish embryos. We found that the temporal shift of Shh activity altered the size of endoskeletal elements in paired fins of zebrafish and dogfish. Thus, a threshold level of hox expression determines the onset of shh expression, and the subsequent heterochronic shift of Shh activity can affect the size of the fin endoskeleton. This process may have facilitated major morphological changes in paired appendages during vertebrate limb evolution.
Conflict of interest statement
Figures
![Figure 1](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2664896/bin/pone.0005121.g001.gif)
![Figure 2](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2664896/bin/pone.0005121.g002.gif)
![Figure 3](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2664896/bin/pone.0005121.g003.gif)
![Figure 4](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2664896/bin/pone.0005121.g004.gif)
![Figure 5](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2664896/bin/pone.0005121.g005.gif)
![Figure 6](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2664896/bin/pone.0005121.g006.gif)
Similar articles
-
Tri-phasic expression of posterior Hox genes during development of pectoral fins in zebrafish: implications for the evolution of vertebrate paired appendages.Dev Biol. 2008 Oct 1;322(1):220-33. doi: 10.1016/j.ydbio.2008.06.032. Epub 2008 Jul 3. Dev Biol. 2008. PMID: 18638469
-
Hedgehog signaling patterns the outgrowth of unpaired skeletal appendages in zebrafish.BMC Dev Biol. 2007 Jun 27;7:75. doi: 10.1186/1471-213X-7-75. BMC Dev Biol. 2007. PMID: 17597528 Free PMC article.
-
Fin development in a cartilaginous fish and the origin of vertebrate limbs.Nature. 2002 Apr 4;416(6880):527-31. doi: 10.1038/416527a. Nature. 2002. PMID: 11932743
-
Fins into limbs: Autopod acquisition and anterior elements reduction by modifying gene networks involving 5'Hox, Gli3, and Shh.Dev Biol. 2016 May 1;413(1):1-7. doi: 10.1016/j.ydbio.2016.03.007. Epub 2016 Mar 15. Dev Biol. 2016. PMID: 26992366 Review.
-
How the embryo makes a limb: determination, polarity and identity.J Anat. 2015 Oct;227(4):418-30. doi: 10.1111/joa.12361. Epub 2015 Aug 7. J Anat. 2015. PMID: 26249743 Free PMC article. Review.
Cited by
-
Comparative analysis of Hmx expression and the distribution of neuronal somata in the trigeminal ganglion in lamprey and shark: insights into the homology of the trigeminal nerve branches and the evolutionary origin of the vertebrate jaw.Zoological Lett. 2023 Dec 5;9(1):23. doi: 10.1186/s40851-023-00222-9. Zoological Lett. 2023. PMID: 38049907 Free PMC article.
-
Spiny and soft-rayed fin domains in acanthomorph fish are established through a BMP-gremlin-shh signaling network.Proc Natl Acad Sci U S A. 2021 Jul 20;118(29):e2101783118. doi: 10.1073/pnas.2101783118. Proc Natl Acad Sci U S A. 2021. PMID: 34230098 Free PMC article.
-
Developmental hourglass and heterochronic shifts in fin and limb development.Elife. 2021 Feb 9;10:e62865. doi: 10.7554/eLife.62865. Elife. 2021. PMID: 33560225 Free PMC article.
-
Sarcopterygian fin ontogeny elucidates the origin of hands with digits.Sci Adv. 2020 Aug 19;6(34):eabc3510. doi: 10.1126/sciadv.abc3510. eCollection 2020 Aug. Sci Adv. 2020. PMID: 32875118 Free PMC article.
-
Transcriptional Landscapes of Divergent Sporophyte Development in Two Mosses, Physcomitrium (Physcomitrella) patens and Funaria hygrometrica.Front Plant Sci. 2020 Jun 10;11:747. doi: 10.3389/fpls.2020.00747. eCollection 2020. Front Plant Sci. 2020. PMID: 32587596 Free PMC article.
References
-
- Sordino P, van der Hoeven F, Duboule D. Hox gene expression in teleost fins and the origin of vertebrate digits. Nature. 1995;375:678–681. - PubMed
-
- Kmita M, Tarchini B, Zakany J, Logan M, Tabin CJ, et al. Early developmental arrest of mammalian limbs lacking HoxA/HoxD gene function. Nature. 2005;435:1113–1116. - PubMed
-
- Tarchini B, Duboule D, Kmita M. Regulatory constraints in the evolution of the tetrapod limb anterior-posterior polarity. Nature. 2006;443:985–988. - PubMed
-
- Thorogood P. The development of the Teleost fin and implications for our understanding of tetrapod limb evolution. In: Hinchliffe JR, Hurle JM, Summerbell D, editors. Developmental Patterning of the Vertebrate Limb. New York: Plenum Pub Corp; 1991.
-
- Saunders JW, Jr, Gasseling MT. Ectoderm-mesenchymal interaction in the origin of wing symmetry. In: Fleischmajer R, Billingham RE, editors. Epithelial–Mesenchymal Interactions. Baltimore: Williams and Wilkins; 1968. pp. 78–97.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Molecular Biology Databases