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A transcriptional time-course analysis of oral vs. aboral whole-body regeneration in the Sea anemone Nematostella vectensis

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ABSTRACT

Background: The ability of regeneration is essential for the homeostasis of all animals as it allows the repair and renewal of tissues and body parts upon normal turnover or injury. The extent of this ability varies greatly in different animals with the sea anemone Nematostella vectensis, a basal cnidarian model animal, displaying remarkable whole-body regeneration competence.

Results: In order to study this process in Nematostella we performed an RNA-Seq screen wherein we analyzed and compared the transcriptional response to bisection in the wound-proximal body parts undergoing oral (head) or aboral (tail) regeneration at several time points up to the initial restoration of the basic body shape. The transcriptional profiles of regeneration responsive genes were analyzed so as to define the temporal pattern of differential gene expression associated with the tissue-specific oral and aboral regeneration. The identified genes were characterized according to their GO (gene ontology) assignations revealing groups that were enriched in the regeneration process with particular attention to their affiliation to the major developmental signaling pathways. While some of the genes and gene groups thus analyzed were previously known to be active in regeneration, we have also revealed novel and surprising candidate genes such as cilia-associated genes that likely participate in this important developmental program.

Conclusions: This work highlighted the main groups of genes which showed polarization upon regeneration, notably the proteinases, multiple transcription factors and the Wnt pathway genes that were highly represented, all displaying an intricate temporal balance between the two sides. In addition, the evolutionary comparison performed between regeneration in different animal model systems may reveal the basic mechanisms playing a role in this fascinating process.

Electronic supplementary material: The online version of this article (doi:10.1186/s12864-016-3027-1) contains supplementary material, which is available to authorized users.

No MeSH data available.


Major Gene Ontology (GO) terms with highly differential oral to aboral expression. Fold change of the most prominent GO terms that are enriched in genes with low concordance between the sides is shown. The numbers next to bars represent Benjamini-Hochberg (BH) adjusted p-values for the enrichment of the GO term
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Fig4: Major Gene Ontology (GO) terms with highly differential oral to aboral expression. Fold change of the most prominent GO terms that are enriched in genes with low concordance between the sides is shown. The numbers next to bars represent Benjamini-Hochberg (BH) adjusted p-values for the enrichment of the GO term

Mentions: Next, we embarked on our main aim of elucidating the molecular basis of the oral vs. aboral (physal) regeneration programs, which is paramount to understanding the nature of the polarized regeneration logic. In order to characterize differentially expressed genes as tissue-specific we tested several methods of correlation analysis of the time course results. We found that the concordance method for correlation calculation (CCC) best revealed differences in both geometry and levels of gene expression. According to this analysis, genes with a low CCC are less similar and more side-specific in their expression pattern. A list of all time course responsive genes in the screen according to their CCC score, together with their oral or aboral nature and their response ratios in the time span of their largest change, is found in Additional file 3: Table S2. For a systematic identification of functional gene groups we considered genes to have a low correlation if they had a CCC of 0.6 or lower and analyzed them for enriched GO terms (as described in Methods). 1804 genes out of the 4205 time responsive genes passed this cutoff. In Table 1 the top most differentially expressed genes out of this list with the above data is shown. It can be clearly observed that the table contains a striking abundance of two types of gene groups: transcription factors and Wnt pathway members. The major GO groups that were detected in the list and their enrichment fold are depicted in Fig. 4 and a full list of the major GO groups with low CCC can be found in Additional file 4: Table S3. Some of the GO categories are redundant while some are a combination of other groups, for instance the large “extracellular region or matrix” groups are composed of the protease/peptidase groups, the Wnt pathway group and the chitin related group. The main functional groups that we found to be enriched among the low concordance genes are described:Table 1


A transcriptional time-course analysis of oral vs. aboral whole-body regeneration in the Sea anemone Nematostella vectensis
Major Gene Ontology (GO) terms with highly differential oral to aboral expression. Fold change of the most prominent GO terms that are enriched in genes with low concordance between the sides is shown. The numbers next to bars represent Benjamini-Hochberg (BH) adjusted p-values for the enrichment of the GO term
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5015328&req=5

Fig4: Major Gene Ontology (GO) terms with highly differential oral to aboral expression. Fold change of the most prominent GO terms that are enriched in genes with low concordance between the sides is shown. The numbers next to bars represent Benjamini-Hochberg (BH) adjusted p-values for the enrichment of the GO term
Mentions: Next, we embarked on our main aim of elucidating the molecular basis of the oral vs. aboral (physal) regeneration programs, which is paramount to understanding the nature of the polarized regeneration logic. In order to characterize differentially expressed genes as tissue-specific we tested several methods of correlation analysis of the time course results. We found that the concordance method for correlation calculation (CCC) best revealed differences in both geometry and levels of gene expression. According to this analysis, genes with a low CCC are less similar and more side-specific in their expression pattern. A list of all time course responsive genes in the screen according to their CCC score, together with their oral or aboral nature and their response ratios in the time span of their largest change, is found in Additional file 3: Table S2. For a systematic identification of functional gene groups we considered genes to have a low correlation if they had a CCC of 0.6 or lower and analyzed them for enriched GO terms (as described in Methods). 1804 genes out of the 4205 time responsive genes passed this cutoff. In Table 1 the top most differentially expressed genes out of this list with the above data is shown. It can be clearly observed that the table contains a striking abundance of two types of gene groups: transcription factors and Wnt pathway members. The major GO groups that were detected in the list and their enrichment fold are depicted in Fig. 4 and a full list of the major GO groups with low CCC can be found in Additional file 4: Table S3. Some of the GO categories are redundant while some are a combination of other groups, for instance the large “extracellular region or matrix” groups are composed of the protease/peptidase groups, the Wnt pathway group and the chitin related group. The main functional groups that we found to be enriched among the low concordance genes are described:Table 1

View Article: PubMed Central - PubMed

ABSTRACT

Background: The ability of regeneration is essential for the homeostasis of all animals as it allows the repair and renewal of tissues and body parts upon normal turnover or injury. The extent of this ability varies greatly in different animals with the sea anemone Nematostella vectensis, a basal cnidarian model animal, displaying remarkable whole-body regeneration competence.

Results: In order to study this process in Nematostella we performed an RNA-Seq screen wherein we analyzed and compared the transcriptional response to bisection in the wound-proximal body parts undergoing oral (head) or aboral (tail) regeneration at several time points up to the initial restoration of the basic body shape. The transcriptional profiles of regeneration responsive genes were analyzed so as to define the temporal pattern of differential gene expression associated with the tissue-specific oral and aboral regeneration. The identified genes were characterized according to their GO (gene ontology) assignations revealing groups that were enriched in the regeneration process with particular attention to their affiliation to the major developmental signaling pathways. While some of the genes and gene groups thus analyzed were previously known to be active in regeneration, we have also revealed novel and surprising candidate genes such as cilia-associated genes that likely participate in this important developmental program.

Conclusions: This work highlighted the main groups of genes which showed polarization upon regeneration, notably the proteinases, multiple transcription factors and the Wnt pathway genes that were highly represented, all displaying an intricate temporal balance between the two sides. In addition, the evolutionary comparison performed between regeneration in different animal model systems may reveal the basic mechanisms playing a role in this fascinating process.

Electronic supplementary material: The online version of this article (doi:10.1186/s12864-016-3027-1) contains supplementary material, which is available to authorized users.

No MeSH data available.