HOX gene complement and expression in the planarian Schmidtea mediterranea

Abstract Background Freshwater planarians are well known for their regenerative abilities. Less well known is how planarians maintain spatial patterning in long-lived adult animals or how they re-pattern tissues during regeneration. HOX genes are good candidates to regulate planarian spatial pattern...

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Main Authors: Ko W. Currie, David D. R. Brown, Shujun Zhu, ChangJiang Xu, Veronique Voisin, Gary D. Bader, Bret J. Pearson
Format: Article
Language:English
Published: BMC 2016-03-01
Series:EvoDevo
Subjects:
HOX
Online Access:http://link.springer.com/article/10.1186/s13227-016-0044-8
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spelling doaj-54f0c1b57c114304a011a67af1f5b9332020-11-24T21:05:42ZengBMCEvoDevo2041-91392016-03-017111110.1186/s13227-016-0044-8HOX gene complement and expression in the planarian Schmidtea mediterraneaKo W. Currie0David D. R. Brown1Shujun Zhu2ChangJiang Xu3Veronique Voisin4Gary D. Bader5Bret J. Pearson6Program in Developmental and Stem Cell Biology, Hospital for Sick ChildrenProgram in Developmental and Stem Cell Biology, Hospital for Sick ChildrenProgram in Developmental and Stem Cell Biology, Hospital for Sick ChildrenDonnelly Centre for Cellular and Biomolecular ResearchDonnelly Centre for Cellular and Biomolecular ResearchDepartment of Molecular Genetics, University of TorontoProgram in Developmental and Stem Cell Biology, Hospital for Sick ChildrenAbstract Background Freshwater planarians are well known for their regenerative abilities. Less well known is how planarians maintain spatial patterning in long-lived adult animals or how they re-pattern tissues during regeneration. HOX genes are good candidates to regulate planarian spatial patterning, yet the full complement or genomic clustering of planarian HOX genes has not yet been described, primarily because only a few have been detectable by in situ hybridization, and none have given morphological phenotypes when knocked down by RNAi. Results Because the planarian Schmidtea mediterranea (S. mediterranea) is unsegmented, appendage less, and morphologically simple, it has been proposed that it may have a simplified HOX gene complement. Here, we argue against this hypothesis and show that S. mediterranea has a total of 13 HOX genes, which represent homologs to all major axial categories, and can be detected by whole-mount in situ hybridization using a highly sensitive method. In addition, we show that planarian HOX genes do not cluster in the genome, yet 5/13 have retained aspects of axially restricted expression. Finally, we confirm HOX gene axial expression by RNA deep-sequencing 6 anterior–posterior “zones” of the animal, which we provide as a dataset to the community to discover other axially restricted transcripts. Conclusions Freshwater planarians have an unappreciated HOX gene complexity, with all major axial categories represented. However, we conclude based on adult expression patterns that planarians have a derived body plan and their asexual lifestyle may have allowed for large changes in HOX expression from the last common ancestor between arthropods, flatworms, and vertebrates. Using our in situ method and axial zone RNAseq data, it should be possible to further understand the pathways that pattern the anterior–posterior axis of adult planarians.http://link.springer.com/article/10.1186/s13227-016-0044-8In situ hybridizationBody planHOXHomeoticLophotrochozoanFlatworm
collection DOAJ
language English
format Article
sources DOAJ
author Ko W. Currie
David D. R. Brown
Shujun Zhu
ChangJiang Xu
Veronique Voisin
Gary D. Bader
Bret J. Pearson
spellingShingle Ko W. Currie
David D. R. Brown
Shujun Zhu
ChangJiang Xu
Veronique Voisin
Gary D. Bader
Bret J. Pearson
HOX gene complement and expression in the planarian Schmidtea mediterranea
EvoDevo
In situ hybridization
Body plan
HOX
Homeotic
Lophotrochozoan
Flatworm
author_facet Ko W. Currie
David D. R. Brown
Shujun Zhu
ChangJiang Xu
Veronique Voisin
Gary D. Bader
Bret J. Pearson
author_sort Ko W. Currie
title HOX gene complement and expression in the planarian Schmidtea mediterranea
title_short HOX gene complement and expression in the planarian Schmidtea mediterranea
title_full HOX gene complement and expression in the planarian Schmidtea mediterranea
title_fullStr HOX gene complement and expression in the planarian Schmidtea mediterranea
title_full_unstemmed HOX gene complement and expression in the planarian Schmidtea mediterranea
title_sort hox gene complement and expression in the planarian schmidtea mediterranea
publisher BMC
series EvoDevo
issn 2041-9139
publishDate 2016-03-01
description Abstract Background Freshwater planarians are well known for their regenerative abilities. Less well known is how planarians maintain spatial patterning in long-lived adult animals or how they re-pattern tissues during regeneration. HOX genes are good candidates to regulate planarian spatial patterning, yet the full complement or genomic clustering of planarian HOX genes has not yet been described, primarily because only a few have been detectable by in situ hybridization, and none have given morphological phenotypes when knocked down by RNAi. Results Because the planarian Schmidtea mediterranea (S. mediterranea) is unsegmented, appendage less, and morphologically simple, it has been proposed that it may have a simplified HOX gene complement. Here, we argue against this hypothesis and show that S. mediterranea has a total of 13 HOX genes, which represent homologs to all major axial categories, and can be detected by whole-mount in situ hybridization using a highly sensitive method. In addition, we show that planarian HOX genes do not cluster in the genome, yet 5/13 have retained aspects of axially restricted expression. Finally, we confirm HOX gene axial expression by RNA deep-sequencing 6 anterior–posterior “zones” of the animal, which we provide as a dataset to the community to discover other axially restricted transcripts. Conclusions Freshwater planarians have an unappreciated HOX gene complexity, with all major axial categories represented. However, we conclude based on adult expression patterns that planarians have a derived body plan and their asexual lifestyle may have allowed for large changes in HOX expression from the last common ancestor between arthropods, flatworms, and vertebrates. Using our in situ method and axial zone RNAseq data, it should be possible to further understand the pathways that pattern the anterior–posterior axis of adult planarians.
topic In situ hybridization
Body plan
HOX
Homeotic
Lophotrochozoan
Flatworm
url http://link.springer.com/article/10.1186/s13227-016-0044-8
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