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C Median expression profiles of clusters in the time courses of regeneration red profiles and budding green profiles. The clusters correspond to figure 3B and the number of genes in each cluster are shown inset. Significance level is at FDR of 0. Clusters 1, 3—4, and 7—8 did not have any enriched GO terms. The PCA analysis of Hydra head regeneration and budding shows that there are sets of genes specific or common to both regeneration and budding time courses.
For a higher resolution analysis to determine these gene sets, we performed a time-series analysis of the regeneration and budding transcriptomes using maSigPro Nueda et al. This analysis identified DE genes that form eight nonredundant clusters fig. DE genes in seven clusters C1 and C3—C8 were expressed at almost steady state during the budding time course but show complex dynamic temporal changes during regeneration fig.
The median expression profiles of DE genes in each cluster are shown in figure 3C. Genes in cluster C2 show gradual temporal activation along both time courses fig. This cluster contains some of the hypostome marker genes such as Wnt1 , ARX , and KS1 that are key developmental genes supplementary fig. The genes in each of the eight distinct clusters fig. Cluster 2, consisting of 72 genes upregulated in mid-to-late stages of both head regeneration and budding, had enriched GO terms related to protein homooligomerization, voltage-gated potassium channel complex, voltage-gated potassium channel activity, potassium ion transport, and transmembrane transport.
Cluster 6 20 genes which increased in expression during regeneration was enriched in endopeptidase inhibitor activity. One of the genes in Cluster 3 was cFos , a transcription factor involved in animal regeneration Petersen et al. ATAC-Seq was also performed during a regeneration time course at hours 0, 2, 4, 6, 12, 24, and 48 fig. We sequenced the ATAC-seq libraries to an average depth of 20 million reads and mapped the reads onto the latest release of the Hydra genome Hydra 2.
Peak calls from each biological replicate were compared and only those that overlapped were retained for downstream analysis. The sets of peaks from all samples in the regeneration time course and body-map were merged to obtain a consolidated set of 27, peaks. We classified the 27, open-chromatin elements according to their genomic locations with respect to the annotated genes.
Using this classification scheme, we identified 9, proximal promoter open elements, 8, intergenic open elements, 6, intronic open elements, and 1, exonic open elements fig. We next looked at the distribution of ATAC-seq signal in the four types of open-chromatin elements defined above supplementary fig. S4 , Supplementary Material online. The proximal promoter open elements possess the highest amount of signal followed by the intergenic open elements. Most of the signal is located at the centers of the four types of peaks.
Based on the genomic locations of the peaks and the enrichment of ATAC-seq signal at them and their distance from the annotated transcription start site TSS , our set of open-chromatin elements provides candidate promoter near TSS and enhancer-like elements intergenic.
A Distribution of open-chromatin elements based on their genomic locations. B The 27, replicated ATAC-seq peaks found in one or more samples were classified based on overlap with gene loci. The proximal promoter regions were defined as regions within 2 kb of start of genes.
In the negative are potential promoters. E Genomic distribution of candidate enhancer-like elements. Using our ATAC-seq data sets, we obtained a set of 27, open-chromatin elements that were classified into four groups based on their genomic locations fig. We used ChIP-seq Schmidl et al. The histone modifications H3K4me3 and H3K4me2 are known to mark chromatin at the promoter regions with a higher ratio of H3K4me3 to H3K4me2, whereas high H3K4me2 with low H3K4me3 predominantly mark the enhancer regions and H3K27ac marks active regulatory regions Perino and Veenstra Correlation analysis of the ChIP-seq approaches found high correlation between replicates and low correlation between different histone modifications supplementary fig.
S5 , Supplementary Material online. For the ATAC-seq data, correlation was in general higher for replicates but high for all samples supplementary fig. S6 , Supplementary Material online. We computed and compared the normalized enrichment of the H3K4me2, H3K4me3, and H3K27ac at the peaks from the four sets of open-chromatin elements classified based on their genomic locations fig.
The proximal promoter open-chromatin elements showed the highest enrichment of H3K4me2, H3K4me3, and H3K27ac with a slightly higher enrichment of H3K4me3 fig. Thus, the chromatin marks provide further evidence for the proximal promoter open-chromatin elements as candidate promoter regions in the Hydra genome.
We expected higher enrichment of H3K4me2 compared with H3K4me3 at the remaining three classes of open-chromatin elements intergenic, intronic, and exonic since these were non-TSS overlapping. We observed almost equal intergenic, fig. A reason for the discrepancy in the relative enrichments of H3K4me2 and H3K4me3 at the non-TSS open-chromatin element sets could be the inclusion of peaks overlapping the nonannotated TSS regions.
Therefore, we used the relative enrichment of H3K4me2 over H3K4me3 to score the peaks and identify candidate enhancer regions fig. Comparison of the histone mark signals at the 3, peaks reveals considerable enrichment of H3K4me2 relative to the H3K4me3 mark fig. Therefore, the set of 3, open-chromatin elements, based on their genomic locations and the enrichment of histone modifications, form the likeliest candidates for enhancer-like regions in the Hydra genome.
Hydra head regeneration is a dynamic process involving changes in expression of multiple genes related to Wnt signaling pathway Lengfeld et al. An important question that remains unanswered is: How extensive is the remodeling of chromatin in Hydra genome in response to bisection and regeneration of a head?
With a genome-wide set of open-chromatin elements obtained from data generated in this study, we explored the above question. Dynamic remodeling of the chromatin during Hydra head regeneration time course can be observed at the Wnt3 gene locus fig. We extended this analysis to the complete set of 27, open-chromatin elements by looking for differentially accessible DA elements genome-wide. The clusters reveal sets of open-chromatin elements specific to certain tissues or head regeneration time course.
For example, cluster 1 consists of open-chromatin elements specific to the foot, budding zone, and BC tissues of Hydra , whereas clusters 3 and 8 consist of elements that lose or gain accessibility during head regeneration respectively fig. Dynamics and motif analysis of 2, DA peaks.
A Normalized reads per million RPM values for the 2, DA peaks were converted to row z scores and k-means clustered into eight clusters based on the observed number of clusters when hierarchically clustered. B Transcription factor-binding motifs enriched in open chromatin regions of each cluster in figure 5A.
We next determined whether the tissue and regeneration time course specific clusters of the 2, DA peaks were enriched for transcription factor-binding sites using Homer Heinz et al. Open chromatin regions of cluster C2 specific to foot, budding zone, BC, and hypostome were enriched for binding site of FoxM1. Open chromatin regions specific to budding zone and BC that lose accessibility along regeneration time course cluster C3 were enriched for the Pax5- and Pax6-binding motifs.
Peak regions in cluster C8 that gain accessibility along the time course of regeneration were enriched for the binding sites of Sox2 and Goosecoid Gsc. The Goosecoid homologue in Hydra is known to participate in head patterning Broun et al. Overall, we found that the nearly ten percent of candidate regulatory elements that show dynamic changes during Hydra head regeneration included clusters that are enriched in predicted transcription factor-binding sites of developmental transcription factors.
We carried out time-course experiments in Hydra using RNA-seq to compare gene expression during head regeneration and budding. We also used ATAC-seq to obtain a genome-wide view of open-chromatin landscape and remodeling in the genome of the adult Hydra body map and during a time course of head regeneration.
To further classify the open-chromatin elements, we carried out ChIP-seq of three histone modifications H3K4me2, H3K4me3, and H3K27ac in a subset of these corresponding samples to annotate the open-chromatin elements as promoter-like or enhancer-like regions. Using these methods, we identified genes that were upregulated in the adult hypostome and may have a role in the head organizer.
We also characterized gene clusters with similar trajectories of expression during head regeneration and budding. We identified two clusters of open chromatin elements that are differentially regulated during head regeneration and identified transcription factor motifs enriched in these clusters.
The time-course RNA-seq experiments in this study has shed light on genome-wide gene expression patterns during formation of the head organizer in Hydra during head regeneration and budding. The head organizer in Hydra is estimated to consist of 50— cells at the apical tip of the head.
Single animal profiling at a greater temporal resolution should provide additional insights into the establishment of head organizer in different developmental scenarios in Hydra and the processes that initiate and maintain it. Whether the head organizer plays a role in sexual embryonic development is not known, although it is likely also involved in the development of the structure of the animal during embryogenesis.
Future extensions of this study to the comparison with the head organizer formation during sexual embryogenesis will reveal the extent of reuse of the normal developmental program during head regeneration. Identification of developmental genes such as Wnt , Ks1 , and ARX upregulated in the adult hypostome and their dynamic expression during regeneration and budding has implications for their role in the head organizer.
As mentioned above, as Hydra grow and cells slough off, the head organizer must continuously be made anew through yet unknown signals and mechanisms. We also predict that these signals increase during head regeneration and budding. Interestingly enough, Wnt1 , ARX , and Ks1 have similar expression patterns that follow what we predict would happen as the head organizer is determined fig.
Wnt3 is expressed in a different cluster due to coming on and peaking much earlier during regeneration and expression decreasing in the adult head fig. In addition, a recent study used single cell sequencing to cluster cells based on cells of different stem cell trajectories Siebert et al. Seibert et al. Wnt1 , Wnt3 , and Wnt7 also show expression in the head ectodermal epithelial cell where Ks1 is expressed.
These results imply that Wnt1 , ARX , and Ks1 maintain head organizer differentiation; they are highly expressed in the adult, expressed during most stages of budding and only in late stages of regeneration once cells have taken on a head organizer role. Wnt3 , while also important to the head organizer and upregulated in the hypostome, is crucial during head regeneration.
Wnt3 is the first gene that comes on and may be triggering an increase of other Wnt and related genes. We propose that Wnt3 is responsible for head organizer cell determination, whereas other genes play a role in head organizer cell differentiation and maintenance.
Petersen et al. They used — animals per each of three replicates. Our results are similar to those of Petersen et al. Their paper and ours are enriched for genes that function in cell signaling and transport. In addition, we found similar patterns of expression for Wnt genes. S2D , Supplementary Material online. Although some of their analyses focused on stem cell factors, we focused on candidate developmental genes discovered by doing a comparison between the hypostome and other tissues.
The genes that we focus on had the highest log-fold change or FDR. Using this method, we uncovered genes that cluster together during regeneration in a transcriptome-wide analysis fig. It should be noted that we used one animal per biological replicate in our RNA-seq study. This may account for differences in patterns of expression for some genes compared with other work using much larger sample sizes, pooled individuals, or increased numbers of replicates.
Characterization and comparisons of gene regulatory networks have gained traction with advances in the field of evolutionary developmental biology evo-devo Carroll The conservation of hox genes highlighted genome similarities across species McGinnis et al. In addition, description of a gene regulatory network with over 40 genes in sea urchin development revealed the role of genome regulation in driving appropriate morphology Davidson et al.
These discoveries bring about questions regarding the role of genome regulation in evolution Hoekstra and Coyne ; Carroll As animal genomes share a lot of similarity in protein coding genes, one theory of evolution suggests that complexity in morphology was driven by complexity of genome regulation. Regeneration of whole structures occurs in a few animal species. The extent to which the genes and gene regulatory networks driving regeneration vary across species remains largely unexplored. In vertebrates, a comparison between a salamander Axolotl and a freshwater fish Polypterus capable of limb and fin regeneration, respectively, found common regeneration-specific genes Darnet et al.
These results demonstrated that in the case of these species the same genetic program coded for structure regeneration. However, the mechanisms underlying regeneration are very different between vertebrates and invertebrates Tanaka and Reddien Recently, it was discovered that an early growth response EGR motif varied in chromatin accessibility during regeneration of the acoel Hofstenia miamia.
By comparing our results of gene regulation and motif-binding during regeneration to that of Hofstenia , we can determine which regenerative programs were present before the divergence of bilaterians. Although we did not find an enrichment for EGR motifs, we found peaks near two of the proposed ten gene targets nlk-like and mtss1-like Gehrke et al. These findings suggest an early role of Fox transcription factors in regeneration of basal species.
Furthermore, although the Fos motif is not enriched as dynamic in Hydra , we found evidence of open chromatin near a gene encoding a Fos protein and we found dynamic expression of a gene encoding a cFos transcription factor fig. Of the genes identified as regeneration-specific in a fish and salamander comparison, one of those genes was FosL2 Gehrke et al.
Our results support the findings of a recent study comparing Hydra head and foot regeneration Cazet et al. Cazet et al. They found no significant differences in chromatic accessibility and gene expression early in regeneration of the Hydra head and foot Cazet et al. Some genes that were previously thought to be head-specific were actually upregulated early in head and foot regeneration and decreased later in foot regeneration.
Similar to our results, Cazet et al. Although the function of FoxM1 in Hydra has not been previously described, we and Cazet et al. In our study, we cannot determine which of our data sets ATAC-seq or histone mark ChIP-seq is more predictive of enhancers due to lack of a gold standard enhancer set in Hydra that could be used to evaluate our data sets. We report 27, candidate regulatory elements, including 3, candidate enhancer-like elements in the Hydra genome, A subset of the identified regulatory elements are dynamically remodeled during head regeneration.
More elements lose accessibility along regeneration time course. We observed the presence of three open elements near the Wnt3 locus: a promoter element that gains accessibility during regeneration and two upstream nonpromoter open elements. Similarly, 12, predicted Hydra genes had at least one nonpromoter regulatory element associated with them, whereas 2, genes had only promoter elements.
Thus, 15, of the total 33, predicted Hydra genes had at least one regulatory element open and detected in our analysis. An important future question is to probe the mode of physical interaction of enhancers and promoters in the cnidarian genomes in the absence of CTCF-mediated DNA looping. Additionally, in this study, we focused on histone marks associated with active regulatory elements.
Future studies on the role of repressive histone marks in gene regulation during important developmental processes, such as head regeneration, can provide further insight. They were fed freshly hatched Artemia salina nauplii twice per week and cultured as described previously Smith et al. For each sample, 1-day starved asexual Hydra polyps were selected.
For regeneration, one animal per sample with two biological replicates was bisected at the region 1 R1 and region 2 R2 border fig. Then the R2—R3 region of the animal only one animal per biological replicate was isolated for RNA extraction. About ng full-length cDNA for each sample was converted to sequencing library by tagmentation with the Illumina Nextera kit.
Eight cycles of PCR were used for library amplification. We used the genome sequence and Augustus predicted gene models from Hydra 2. Adapter sequences and low-quality base pairs from the paired-ends reads were trimmed using Trimmomatic v. The transcripts per millions TPM values were then smooth quantile normalized using qsmooth package Hicks et al. Time-series analysis of budding and head regeneration time courses was done using maSigPro v.
The heatmap of DE genes fig. The TPM values of the DE genes were log2 transformed and converted to z scores for clustering and generating heatmap. Annotations on the heatmaps were done in Adobe illustrator Adobe Inc. S3, S5, and S6 , Supplementary Material online. Each maSigPro cluster of DE genes fig. The GO enrichment analysis was performed using the entire transcriptome as the reference set. To identify genes and functions unique to the different body parts of Hydra , we did a differential expression analysis and GO term annotation of genes upregulated in Hydra tentacles, hypostome, BC, budding zone, and foot.
We identified DE genes by doing ten pairwise comparisons between two different tissues in edgeR Robinson et al. We merged results of each pairwise comparison to identify genes uniquely upregulated in each of the five tissues supplementary table S1 , Supplementary Material online. Upregulated genes were annotated with potential functions using Blast2GO Conesa et al.
For chromatin profiling experiments using ATAC-seq, the Hydra polyps were first incubated in a cocktail of four antibiotics for one week with feeding, followed by one week of recovery in sterile medium according to the protocol by Fraune et al. For regeneration, 20 animals per sample with two biological replicates were bisected at the region 1 R1 and region 2 R2 border fig. Then the R2 regions of the animals of a sample were isolated for nuclei isolation and tagmentation ATAC-seq or crosslinking and immunoprecipitation.
Nuclei from tissues described in the previous section were isolated using the following protocol based on Endl et al. Briefly, Hydra tissues were washed in ice-cold PBS once. The supernatant was removed. Sequencing library qualities were assessed using a Bioanalyzer and the libraries were sequenced as bp paired-end reads on an Illumina NextSeq Each sample was performed with two biological replicates. The sequencing libraries were prepared according to protocol.
Sequencing library qualities were assessed on Bioanalyzer and the libraries were sequenced as bp paired-end reads on an Illumina NextSeq Each experiment was performed with two biological replicates. The trimmed paired-end reads were first mapped to Hydra mitochondrial DNA sequences to filter the mitochondrial reads.
The unmapped reads were mapped to the genome sequence from Hydra 2. Peaks were called using Homer v. The peaks from all samples were merged using Bedtools v. The read counts for each sample were normalized for efficiency number of reads within peaks divided by total number of mapped reads and sequencing depth. The trimmed paired-end reads were mapped to the genome sequence from Hydra 2. The read counts for each sample were normalized for efficiency and sequencing depth.
Supplementary data are available at Genome Biology and Evolution online. We would like to thank Rob Steele for input in Hydra handling and experimental design. This work was supported in part by a George E. Hewitt Foundation for Medical Research felllowship to A. The raw and processed sequencing data reported in this manuscript are deposited in GEO under the main accession number GSE Differentiation 74 6 : — Google Scholar.
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Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. So far, only one sponge cadherin gene that encodes a cytoplasmic domain with weak similarity to the eumetazoan CCD domain has been detected. The sequencing of the Hydra genome has revealed unexpected relationships between the genetic makeup of the animal and its biology. The genes encoding the proteins that form epithelial junctions in bilaterians are present in Hydra yet there are obvious differences in structures of the junctional complexes.
Despite the morphological similarity of neuromuscular junctions in bilaterians and Hydra , several of the key genes required to make this junction in bilaterians are absent from Hydra. Hydra has a complete set of muscle genes but lacks mesoderm and forms muscles only in epithelial cells.
Most of the genes required for stem cell pluripotency in mammals are absent from Hydra , yet Hydra has a multipotent stem cell system that functions similarly to stem cell systems in bilaterians. The availability of the Hydra genome sequence and methods to manipulate it 30 provide an opportunity to understand how this remarkable animal evolved.
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Download references. We are grateful to S. Clifton, R. We thank J. The septate junction electron micrograph in Fig. Melmon and the Gordon and Betty Moore Foundation. Support for H. Support for A. Mercator Professor and Y. Author Contributions J. Nicholas H. Putnam, Philip A. Jarrod A. Chapman, Ewen F. Kirkness and Oleg Simakov: These authors contributed equally to this work. Chapman, David M.
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Download PDF. Subjects Genome Model invertebrates. Abstract The freshwater cnidarian Hydra was first described in 1 and has been the object of study for years. Main The genomic basis of cnidarian evolution has so far been viewed from the perspective of an anthozoan, the sea anemone Nematostella vectensis 6.
Hydra transcription незаконная культивация коноплиThe Undying Hydra: A Freshwater Mini-Monster That Defies Aging - Deep Look
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