A conserved cluster of three PRD-class homeobox genes (<it>homeobrain</it>, <it>rx </it>and <it>orthopedia</it>) in the Cnidaria and Protostomia
<p>Abstract</p> <p>Background</p> <p>Homeobox genes are a superclass of transcription factors with diverse developmental regulatory functions, which are found in plants, fungi and animals. In animals, several Antennapedia (ANTP)-class homeobox genes reside in extremely...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
BMC
2010-07-01
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| Series: | EvoDevo |
| Online Access: | http://www.evodevojournal.com/content/1/1/3 |
| _version_ | 1818114494470029312 |
|---|---|
| author | Mazza Maureen E Pang Kevin Reitzel Adam M Martindale Mark Q Finnerty John R |
| author_facet | Mazza Maureen E Pang Kevin Reitzel Adam M Martindale Mark Q Finnerty John R |
| author_sort | Mazza Maureen E |
| collection | DOAJ |
| description | <p>Abstract</p> <p>Background</p> <p>Homeobox genes are a superclass of transcription factors with diverse developmental regulatory functions, which are found in plants, fungi and animals. In animals, several Antennapedia (ANTP)-class homeobox genes reside in extremely ancient gene clusters (for example, the Hox, ParaHox, and NKL clusters) and the evolution of these clusters has been implicated in the morphological diversification of animal bodyplans. By contrast, similarly ancient gene clusters have not been reported among the other classes of homeobox genes (that is, the LIM, POU, PRD and SIX classes).</p> <p>Results</p> <p>Using a combination of <it>in silico </it>queries and phylogenetic analyses, we found that a cluster of three PRD-class homeobox genes (<it>Homeobrain (hbn)</it>, <it>Rax (rx) </it>and <it>Orthopedia (otp)</it>) is present in cnidarians, insects and mollusks (a partial cluster comprising hbn and rx is present in the placozoan <it>Trichoplax adhaerens</it>). We failed to identify this 'HRO' cluster in deuterostomes; in fact, the <it>Homeobrain </it>gene appears to be missing from the chordate genomes we examined, although it is present in hemichordates and echinoderms. To illuminate the ancestral organization and function of this ancient cluster, we mapped the constituent genes against the assembled genome of a model cnidarian, the sea anemone <it>Nematostella vectensis</it>, and characterized their spatiotemporal expression using <it>in situ </it>hybridization. In <it>N. vectensis</it>, these genes reside in a span of 33 kb with the same gene order as previously reported in insects. Comparisons of genomic sequences and expressed sequence tags revealed the presence of alternative transcripts of Nv-otp and two highly unusual protein-coding polymorphisms in the terminal helix of the Nv-rx homeodomain. A population genetic survey revealed the Rx polymorphisms to be widespread in natural populations. During larval development, all three genes are expressed in the ectoderm, in non-overlapping territories along the oral-aboral axis, with distinct temporal expression.</p> <p>Conclusion</p> <p>We report the first evidence for a PRD-class homeobox cluster that appears to have been conserved since the time of the cnidarian-bilaterian ancestor, and possibly even earlier, given the presence of a partial cluster in the placozoan <it>Trichoplax</it>. Very similar clusters comprising these three genes exist in <it>Nematostella </it>and diverse protostomes. Interestingly, in chordates, one member of the ancestral cluster (<it>homeobrain</it>) has apparently been lost, and there is no linkage between <it>rx </it>and <it>orthopedia </it>in any of the vertebrates. In <it>Nematostella</it>, the spatial expression of these three genes along the body column is not colinear with their physical order in the cluster but the temporal expression is, therefore, using the terminology that has been applied to the Hox cluster genes, the HRO cluster would appear to exhibit temporal but not spatial colinearity. It remains to be seen whether the mechanisms responsible for the evolutionary conservation of the HRO cluster are the same mechanisms responsible for cohesion of the Hox cluster and other ANTP-class homeobox clusters that have been widely conserved throughout animal evolution.</p> |
| first_indexed | 2024-12-11T03:51:37Z |
| format | Article |
| id | doaj.art-1a3f6749465348f6a1104f6ce1fb6034 |
| institution | Directory Open Access Journal |
| issn | 2041-9139 |
| language | English |
| last_indexed | 2024-12-11T03:51:37Z |
| publishDate | 2010-07-01 |
| publisher | BMC |
| record_format | Article |
| series | EvoDevo |
| spelling | doaj.art-1a3f6749465348f6a1104f6ce1fb60342022-12-22T01:21:52ZengBMCEvoDevo2041-91392010-07-0111310.1186/2041-9139-1-3A conserved cluster of three PRD-class homeobox genes (<it>homeobrain</it>, <it>rx </it>and <it>orthopedia</it>) in the Cnidaria and ProtostomiaMazza Maureen EPang KevinReitzel Adam MMartindale Mark QFinnerty John R<p>Abstract</p> <p>Background</p> <p>Homeobox genes are a superclass of transcription factors with diverse developmental regulatory functions, which are found in plants, fungi and animals. In animals, several Antennapedia (ANTP)-class homeobox genes reside in extremely ancient gene clusters (for example, the Hox, ParaHox, and NKL clusters) and the evolution of these clusters has been implicated in the morphological diversification of animal bodyplans. By contrast, similarly ancient gene clusters have not been reported among the other classes of homeobox genes (that is, the LIM, POU, PRD and SIX classes).</p> <p>Results</p> <p>Using a combination of <it>in silico </it>queries and phylogenetic analyses, we found that a cluster of three PRD-class homeobox genes (<it>Homeobrain (hbn)</it>, <it>Rax (rx) </it>and <it>Orthopedia (otp)</it>) is present in cnidarians, insects and mollusks (a partial cluster comprising hbn and rx is present in the placozoan <it>Trichoplax adhaerens</it>). We failed to identify this 'HRO' cluster in deuterostomes; in fact, the <it>Homeobrain </it>gene appears to be missing from the chordate genomes we examined, although it is present in hemichordates and echinoderms. To illuminate the ancestral organization and function of this ancient cluster, we mapped the constituent genes against the assembled genome of a model cnidarian, the sea anemone <it>Nematostella vectensis</it>, and characterized their spatiotemporal expression using <it>in situ </it>hybridization. In <it>N. vectensis</it>, these genes reside in a span of 33 kb with the same gene order as previously reported in insects. Comparisons of genomic sequences and expressed sequence tags revealed the presence of alternative transcripts of Nv-otp and two highly unusual protein-coding polymorphisms in the terminal helix of the Nv-rx homeodomain. A population genetic survey revealed the Rx polymorphisms to be widespread in natural populations. During larval development, all three genes are expressed in the ectoderm, in non-overlapping territories along the oral-aboral axis, with distinct temporal expression.</p> <p>Conclusion</p> <p>We report the first evidence for a PRD-class homeobox cluster that appears to have been conserved since the time of the cnidarian-bilaterian ancestor, and possibly even earlier, given the presence of a partial cluster in the placozoan <it>Trichoplax</it>. Very similar clusters comprising these three genes exist in <it>Nematostella </it>and diverse protostomes. Interestingly, in chordates, one member of the ancestral cluster (<it>homeobrain</it>) has apparently been lost, and there is no linkage between <it>rx </it>and <it>orthopedia </it>in any of the vertebrates. In <it>Nematostella</it>, the spatial expression of these three genes along the body column is not colinear with their physical order in the cluster but the temporal expression is, therefore, using the terminology that has been applied to the Hox cluster genes, the HRO cluster would appear to exhibit temporal but not spatial colinearity. It remains to be seen whether the mechanisms responsible for the evolutionary conservation of the HRO cluster are the same mechanisms responsible for cohesion of the Hox cluster and other ANTP-class homeobox clusters that have been widely conserved throughout animal evolution.</p>http://www.evodevojournal.com/content/1/1/3 |
| spellingShingle | Mazza Maureen E Pang Kevin Reitzel Adam M Martindale Mark Q Finnerty John R A conserved cluster of three PRD-class homeobox genes (<it>homeobrain</it>, <it>rx </it>and <it>orthopedia</it>) in the Cnidaria and Protostomia EvoDevo |
| title | A conserved cluster of three PRD-class homeobox genes (<it>homeobrain</it>, <it>rx </it>and <it>orthopedia</it>) in the Cnidaria and Protostomia |
| title_full | A conserved cluster of three PRD-class homeobox genes (<it>homeobrain</it>, <it>rx </it>and <it>orthopedia</it>) in the Cnidaria and Protostomia |
| title_fullStr | A conserved cluster of three PRD-class homeobox genes (<it>homeobrain</it>, <it>rx </it>and <it>orthopedia</it>) in the Cnidaria and Protostomia |
| title_full_unstemmed | A conserved cluster of three PRD-class homeobox genes (<it>homeobrain</it>, <it>rx </it>and <it>orthopedia</it>) in the Cnidaria and Protostomia |
| title_short | A conserved cluster of three PRD-class homeobox genes (<it>homeobrain</it>, <it>rx </it>and <it>orthopedia</it>) in the Cnidaria and Protostomia |
| title_sort | conserved cluster of three prd class homeobox genes it homeobrain it it rx it and it orthopedia it in the cnidaria and protostomia |
| url | http://www.evodevojournal.com/content/1/1/3 |
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