Analysis of distribution of chromatin marks across &quot;divergence islands&quot; in three-spined stickleback (<i>Gasterosteus aculeatus</i>)

Alexey Sokolov; Svetlana Zhenilo; Sergey Rastorguev; Alexander Mazur; Egor Prokhortchouk

doi:10.12688/f1000research.10428.1

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Research Note

Analysis of distribution of chromatin marks across "divergence islands" in three-spined stickleback (Gasterosteus aculeatus)

[version 1; peer review: 2 approved with reservations]

Alexey Sokolov ¹, Svetlana Zhenilo¹, Sergey Rastorguev², Alexander Mazur¹, Egor Prokhortchouk¹

Alexey Sokolov ¹, Svetlana Zhenilo¹, [...] Sergey Rastorguev², Alexander Mazur¹, Egor Prokhortchouk¹

PUBLISHED 20 Dec 2016

Author details Author details

¹ Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow, Russian Federation
² National Research Center 'Kurchatov Institute', Moscow, Russian Federation

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Abstract

The three-spined stickleback (Gasterosteus aculeatus) is a well-known model organism for studying adaptations to water salinity. In this work, we investigate the dynamics of an epigenetic landscape of water salinity adaptation using three chromatin marks: H3K27ac, H3K4me1 and H3K4me3. The choice of marks was determined by the fact that some adaptive genomic loci are situated in gene-free regions, suggesting their regulatory role as enhancers. Histone modifications seem to be a promising mechanism that could regulate such regions. Difference between histone modifications in sea and freshwater - both in genes and intergenic enhancers - may contribute to epigenetic plasticity of stickleback adaptation. As a result of this study, we found differential chromatin peaks in "divergence islands" at enhancer elements and promoters of genes, which are responsible for stress adaptation and homeostasis. However, a full genome study analysis is required to fully understand mechanism of adaptation to water salinity.

Keywords

divergence islands, chromatin marks, Gasterosteus aculeatus

Corresponding author: Alexey Sokolov

Competing interests: The authors declare no conflict of interest.

Grant information: This work was supported by the Russian Science Foundation (RSF; grant #14-24-00175).

Copyright: © 2016 Sokolov A et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: Sokolov A, Zhenilo S, Rastorguev S et al. Analysis of distribution of chromatin marks across "divergence islands" in three-spined stickleback (Gasterosteus aculeatus) [version 1; peer review: 2 approved with reservations]. F1000Research 2016, 5:2880 (https://doi.org/10.12688/f1000research.10428.1) First published: 20 Dec 2016, 5:2880 (https://doi.org/10.12688/f1000research.10428.1) Latest published: 20 Dec 2016, 5:2880 (https://doi.org/10.12688/f1000research.10428.1)

Introduction

The three-spined stickleback (Gasterosteus aculeatus) is a model organism that can be used to elucidate molecular mechanisms of adaption to various salinities. In this work, we analyze epigenetic signatures that can be specific for various salinities. We study three chromatin marks H3K27ac, H3K4me1 and H3K4me3, which were chosen as these marks label active enhancers and promoters¹, in marine and fresh water sticklebacks in their natural habitats, as well as in foreign (change of salinity) environments. These marks were studied in 19 “divergence islands”², short genomic regions, which are highly diverged between marine and fresh water species. In the present study, 17 divergence islands overlapped in protein-coding genes, which are relevant to fresh water adaptation. In addition, we report the changes of histone modifications between marine and freshwater fish in promoters of protein-coding genes and enhancers.

Methods

Sample preparation and ChIP experiment

In this study, we used six marine and six fresh water sticklebacks, which were collected in august of 2015 from the White Sea (near the Pertsov White Sea Biological Station of Lomonosov Moscow State University, Murmanskaya Oblast, Russia) and Mashinnoe Lake (located near the village of Chkalvosky, Repuyblic of Karelia, Russia), respectively. The fish were placed for four days in various water tanks: half of the sticklebacks from each group was kept in the water with their natural salinity (FF and MM for fresh and marine water, respectively) and the other half was kept in a modified environment (i.e. three fresh water fish was placed in salty water (FM) and three marine fish were placed in fresh water (MF)). The live fish were transferred to the laboratory to Moscow.

For the chromatin immunoprecipitation (ChIP)-seq experiments, gills were collected from all 12 sticklebacks. Chromatin was prepared from gills, as described by Cell Signalling (https://www.cellsignal.com/common/content/content.jsp?id=chip-agarose) and ChIP was performed as described by Filion et al.³.

Bioinformatics analysis

Reads were aligned to gasAcu1 reference genome from the UCSC Genome Browser Gateway (https://genome-euro.ucsc.edu/) by Bowtie2 (http://bowtie-bio.sourceforge.net/bowtie2/index.shtml) with a "very-sensitive-local" parameter^4,5. For peaks calling we used MACS version 1.4.2⁶. For the intersection of peaks with divergence islands and genes we used bedtools version 2.26.0⁷.

Results

In our study, we determined between 7138 and 20828 histone modification peaks (Table 1). We selected histone modification peaks in “divergence islands” regions, which are highly divergent between marine and freshwater populations of sticklebacks². We observed that the majority (17 out of 19) of the islands showed the same chromatin marks (H3K4me1, H3K4me3 and H3K27ac) in fresh water species in their natural salinity (FF) and fresh water species placed into a marine environment (FM). The same was true for marine water species in their natural salinity (MM) and marine water species placed into a fresh water environment (MF). In addition, the majority of the islands (14 out of 19) showed the same histone modifications between the whole set of marine and fresh water species (MM+MF vs. FF+FM; Table 2).

Table 1. Results of reads mapping and peaks calling.

MM - marine species in natural environment; MF - marine species in fresh water; FF - fresh water species in natural environment; FM - fresh water species in marine water.

SamFle Name	All reads	Mapped reads	Ratio	Peaks
MMH3K27ac	16,319,162	13,242,763	81.14854795	11906
MMH3K4me1	15,805,735	12,244,401	77.46808991	13289
MMH3K4me3	7,354,166	6,872,442	93.44964473	12944
MFH3K27ac	16,917,583	9,700,338	57.33879361	13964
MFH3K4me1	12,773,849	10,303,455	80.66053544	20828
MFH3K4me3	14,099,289	7,836,369	55.57988775	18851
FFH3K27ac	14,567,425	11,367,244	78.0319377	9130
FFH3K4me1	12,243,305	10,737,653	87.70224216	8825
FFH3K4me3	15,176,697	9,476,326	62.43997623	14672
FMH3K27ac	14,850,800	11,887,597	80.04684596	12889
FMH3K4me1	13,213,512	10,426,786	78.91002786	7138
FMH3K4me3	14,512,630	11,658,225	80.33158015	15723

Table 2. Results of intersection of chromatin peaks with divergence islands and differential chromatin peaks analysis between MM and MF, and between FF and FM.

“0” - no intersection; “1” – intersection. Regions with differential chromatin peaks are highlighted. MM - marine species in natural environment; MF - marine species in fresh water; FF - fresh water species in natural environment; FM - fresh water species in marine water. Differential peaks islands are highlighted in red.

Divergence islands coordinates			MM			MF			FF			FM
Chromosome	Start	End	H3K27ac	H3K4me1	H3K4me3	H3K27ac	H3K4me1	H3K4me3	H3K27ac	H3K4me1	H3K4me3	H3K27ac	H3K4me1	H3K4me3
chrI	21,487,998	21,960,119	1	1	1	1	1	1	1	1	1	1	1	1
chrII	14,874,366	14,898,826	0	0	0	0	0	0	0	0	0	0	0	0
chrIV	12,803,780	12,881,296	1	1	1	1	1	1	1	1	1	1	1	1
chrIV	13,930,002	13,959,331	0	1	0	0	1	1	0	1	1	0	1	1
chrIV	19,811,922	19,914,666	1	1	1	1	1	1	1	1	1	1	1	1
chrIV	23,954,634	23,981,981	1	0	1	1	1	1	1	0	1	1	0	1
chrIV	26,016,955	26,166,536	1	1	1	1	1	1	1	1	1	1	1	1
chrV	2,482,209	2,501,295	1	1	1	1	1	1	1	0	1	1	0	1
chrVII	17,982,351	18,002,671	1	1	1	1	1	1	1	1	1	1	1	1
chrIX	8,521,935	8,537,559	1	1	1	1	1	1	1	1	1	1	0	1
chrIX	8,901,816	8,910,115	1	1	1	1	1	1	0	0	1	1	0	1
chrIX	9,208,158	9,227,809	0	0	0	0	0	0	0	0	0	0	0	0
chrIX	10334101	10353801	1	1	1	1	1	1	0	0	1	0	1	1
chrXI	5445757	5855124	1	1	1	1	1	1	1	1	1	1	1	1
chrXII	14338229	14358336	1	1	1	1	1	1	1	0	1	1	0	1
chrXII	16522028	16538810	0	0	0	0	0	0	0	0	0	0	0	0
chrXIX	2449903	2581858	1	1	1	1	1	1	1	1	1	1	1	1
chrXIX	14787904	14799088	0	0	0	0	0	0	0	0	0	0	0	0
chrXXI	5759879	7486635	1	1	1	1	1	1	1	1	1	1	1	1

Nevertheless, we found 3 out of 19 “divergence islands” demonstrating differential chromatin marks in cases of short-term adaptation to water salinity for fish placed into foreign environments. Interestingly, one “divergence island” gained H3K4me1 in the promoter of the RPTOR gene in FM. The other two islands gained H3K27ac and lost H3K4me1 inf FM, suggesting their role as enhancers for genes outside the island. Also, two islands gained H3K4me3 and H3K4me1 at STC2 and PNPLA3 genes, respectively, in MF.

Finally, 5 out of 19 islands demonstrated differential histone modifications between fresh water species and marine species placed into fresh water (FF vs MF) (Table 3). In all these cases, MF gained a mark, which was absent in a FF. For example, H3K4me1 was gained in LRRC59 and BDH2 genes, which is involved in the adaption to stress and homeostasis⁸, suggesting that these genes might be activated after the placement of marine fish into a fresh water environment. In addition, 6 islands out of 19 demonstrated differential histone modifications between marine and fresh water species placed in marine water, with both gains and losses of marks (Table 3). Among these, we found that H3K4me3 was gained at STC2 in FM* compared to MM*, H3K4me1 at LRRC59 and BDH2 in MM* compared with FM*, and H3K27ac at RPTR in MM* compared with FM*.

Table 3. Results of intersection of chromatin peaks with divergence islands and differential chromatin peaks analysis between FM and MM, and between MF and FF.

“0” - no intersection; “1” – intersection. Regions with differential chromatin peaks are highlighted. MM - marine species in natural environment; MF - marine species in fresh water; FF - fresh water species in natural environment; FM - fresh water species in marine water. Differential peaks islands are highlighted in red.

Divergence islands coordinates			FM			MM			MF			FF
Chromosome	Start	End	H3K27ac	H3K4me1	H3K4me3	H3K27ac	H3K4me1	H3K4me3	H3K27ac	H3K4me1	H3K4me3	H3K27ac	H3K4me1	H3K4me3
chrI	21,487,998	21,960,119	1	1	1	1	1	1	1	1	1	1	1	1
chrII	14,874,366	14,898,826	0	0	0	0	0	0	0	0	0	0	0	0
chrIV	12,803,780	12,881,296	1	1	1	1	1	1	1	1	1	1	1	1
chrIV	13,930,002	13,959,331	0	1	1	0	1	0	0	1	1	0	1	1
chrIV	19,811,922	19,914,666	1	1	1	1	1	1	1	1	1	1	1	1
chrIV	23,954,634	23,981,981	1	0	1	1	0	1	1	1	1	1	0	1
chrIV	26,016,955	26,166,536	1	1	1	1	1	1	1	1	1	1	1	1
chrV	2,482,209	2,501,295	1	0	1	1	1	1	1	1	1	1	0	1
chrVII	17,982,351	18,002,671	1	1	1	1	1	1	1	1	1	1	1	1
chrIX	8,521,935	8,537,559	1	0	1	1	1	1	1	1	1	1	1	1
chrIX	8,901,816	8,910,115	1	0	1	1	1	1	1	1	1	0	0	1
chrIX	9,208,158	9,227,809	0	0	0	0	0	0	0	0	0	0	0	0
chrIX	10334101	10353801	0	1	1	1	1	1	1	1	1	0	0	1
chrXI	5445757	5855124	1	1	1	1	1	1	1	1	1	1	1	1
chrXII	14338229	14358336	1	0	1	1	1	1	1	1	1	1	0	1
chrXII	16522028	16538810	0	0	0	0	0	0	0	0	0	0	0	0
chrXIX	2449903	2581858	1	1	1	1	1	1	1	1	1	1	1	1
chrXIX	14787904	14799088	0	0	0	0	0	0	0	0	0	0	0	0
chrXXI	5759879	7486635	1	1	1	1	1	1	1	1	1	1	1	1

Conclusions

In this study, we analyzed the epigenetic profile of "divergence islands" with three chromatin marks, H3K4me1, H3K4me3 and H3K27ac. We report differential histone modifications that might be involved in the regulation of promoters and enhancers located in "divergent islands", and therefore contribute to adaptation to water salinity. Furthermore, we found differential chromatin peaks at promoters of genes that are responsible for stress adaptation and homeostasis. The results of this study contributes to our understanding of molecular mechanisms of adaptation to water salinity. However, a full genome histone modification analysis is required in order to further understand these mechanisms of adaptation.

Data availability

Fastq files can be found in the SRA archive under accession number SRX2403902 (https://www.ncbi.nlm.nih.gov/sra/?term=SRX2403902).

Author contributions

SR designed the experiment. SZ and AM prepared ChIP-seq libraries. AS and EP carried out the research. AS wrote the manuscript.

Competing interests

The authors declare no conflict of interest.

Grant information

This work was supported by the Russian Scientific Foundation (RSF; grant #14-24-00175).

Acknowledgements

The authors are grateful to Konstantin G. Skryabin and Yulia Medvedeva (Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences) for ongoing support and valuable comments throughout the preparation of the manuscript.

F1000 recommended

References

1. Shlyueva D, Stampfel G, Stark A: Transcriptional enhancers: from properties to genome-wide predictions. Nat Rev Genet. 2014; 15(4): 272–286. PubMed Abstract | Publisher Full Text
2. Terekhanova NV, Logacheva MD, Penin AA, et al.: Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLoS Genet. 2014; 10(10): e1004696. PubMed Abstract | Publisher Full Text | Free Full Text
3. Filion GJ, Zhenilo S, Salozhin S, et al.: A family of human zinc finger proteins that bind methylated DNA and repress transcription. Mol Cell Biol. 2006; 26(1): 169–81. PubMed Abstract | Publisher Full Text | Free Full Text
4. Langmead B, Salzberg SL: Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9(4): 357–359. PubMed Abstract | Publisher Full Text | Free Full Text
5. Langmead B, Trapnell C, Pop M, et al.: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10(3): R25. PubMed Abstract | Publisher Full Text | Free Full Text
6. Zhang Y, Liu T, Meyer CA, et al.: Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008; 9(9): R137. PubMed Abstract | Publisher Full Text | Free Full Text
7. Quinlan AR, Hall IM: BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010; 26(6): 841–842. PubMed Abstract | Publisher Full Text | Free Full Text
8. Devireddy LR, Hart DO, Goetz DH, et al.: A mammalian siderophore synthesized by an enzyme with a bacterial homolog involved in enterobactin production. Cell. 2010; 141(6): 1006–17. PubMed Abstract | Publisher Full Text | Free Full Text

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Author details Author details

¹ Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow, Russian Federation
² National Research Center 'Kurchatov Institute', Moscow, Russian Federation

Competing interests

The authors declare no conflict of interest.

Grant information

This work was supported by the Russian Science Foundation (RSF; grant #14-24-00175).

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Published: 20 Dec 2016, 5:2880

https://doi.org/10.12688/f1000research.10428.1

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© 2016 Sokolov A et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Sokolov A, Zhenilo S, Rastorguev S et al. Analysis of distribution of chromatin marks across "divergence islands" in three-spined stickleback (Gasterosteus aculeatus) [version 1; peer review: 2 approved with reservations]. F1000Research 2016, 5:2880 (https://doi.org/10.12688/f1000research.10428.1)

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Reviewer Report 20 Mar 2017

Ilkka Kronholm, Centre of Excellence in Biological Interactions, Department of Biological and Environmental Sciences, University of Jyväskylä, Jyväskylä, Finland

Approved with Reservations

https://doi.org/10.5256/f1000research.11237.r20811

The study by Sokolov et al. investigates changes in chromatin marks among saline and freshwater populations of sticklebacks. While I like the idea of the study and I do appreciate that this manuscript is intended as a short note, the ... Continue reading

The study by Sokolov et al. investigates changes in chromatin marks among saline and freshwater populations of sticklebacks. While I like the idea of the study and I do appreciate that this manuscript is intended as a short note, the current state of this manuscript is not suitable for indexing at the moment. The authors need to rewrite most of the manuscript as major revision is necessary. I've given some suggestions below.

Introduction
The introduction needs to be expanded so that the authors give some background on the system as well, there is plenty of previous research on the stickleback system that has been done and more of it needs to be cited here. Please also explain the ideas behind the divergence islands, give some information about these chromatin marks etc.

Methods
More information needs to be given about the chromatin immunoprecipitation experiments and the bioinformatic analysis. Currently the methods do not stand on their own. For example, at the moment the manuscript only states that MACS software was used for peak calling with no information how the method works or what parameters were used.

Results
I was wondering would it be helpful if the some of the results were shown as figures. Perhaps at least those peaks where differences were found.

Discussion
Currently the results are not really discussed at all. The authors should properly discuss their results. The authors found changes in certain genes, but the biological functions of those genes are barely mentioned or whether these are candidates for explaining adaptation to marine and freshwater environments.

Competing Interests: No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Reviewer Report 03 Jan 2017

Alexey Ruzov, Division of Cancer and Stem Cells, Centre for Biomolecular Sciences (CBS), School of Medicine, University of Nottingham, Nottingham, UK

Approved with Reservations

https://doi.org/10.5256/f1000research.11237.r18627

In my opinion, the results on differential distribution of histone modifications in sea and freshwater three-spined sticklebacks may potentially be interesting. Despite this, I strongly believe that text of the manuscript is currently beyond the minimal standards required for paper indexing.
... Continue reading

In my opinion, the results on differential distribution of histone modifications in sea and freshwater three-spined sticklebacks may potentially be interesting. Despite this, I strongly believe that text of the manuscript is currently beyond the minimal standards required for paper indexing.

Specifically: the abstract does not describe main findings of the paper in sufficient detail; the introduction does not provide an adequate background information for the study but, instead, mainly repeats the abstract; any Discussion comparing the results with already available literature is missing; some crucial details of the methodologies used (e.g. which antibodies have been used for CHIP) are missing from Methods; some sentences in the text are difficult to understand.

I recommend the authors to rewrite the text of manuscript addressing these points.

Competing Interests: No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Alexey Ruzov, University of Nottingham, Nottingham, UK
Ilkka Kronholm, University of Jyväskylä, Jyväskylä, Finland

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20 Mar 2017 | for Version 1

Ilkka Kronholm, Centre of Excellence in Biological Interactions, Department of Biological and Environmental Sciences, University of Jyväskylä, Jyväskylä, Finland

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Approved With Reservations

The study by Sokolov et al. investigates changes in chromatin marks among saline and freshwater populations of sticklebacks. While I like the idea of the study and I do appreciate that this manuscript is intended as a short note, the current state of this manuscript is not suitable for indexing at the moment. The authors need to rewrite most of the manuscript as major revision is necessary. I've given some suggestions below.

Introduction
The introduction needs to be expanded so that the authors give some background on the system as well, there is plenty of previous research on the stickleback system that has been done and more of it needs to be cited here. Please also explain the ideas behind the divergence islands, give some information about these chromatin marks etc.

Methods
More information needs to be given about the chromatin immunoprecipitation experiments and the bioinformatic analysis. Currently the methods do not stand on their own. For example, at the moment the manuscript only states that MACS software was used for peak calling with no information how the method works or what parameters were used.

Results
I was wondering would it be helpful if the some of the results were shown as figures. Perhaps at least those peaks where differences were found.

Discussion
Currently the results are not really discussed at all. The authors should properly discuss their results. The authors found changes in certain genes, but the biological functions of those genes are barely mentioned or whether these are candidates for explaining adaptation to marine and freshwater environments.

Competing Interests

No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Respond to this report

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Reviewer Report

20 Views

03 Jan 2017 | for Version 1

Alexey Ruzov, Division of Cancer and Stem Cells, Centre for Biomolecular Sciences (CBS), School of Medicine, University of Nottingham, Nottingham, UK

20 Views Cite this report Responses(0)

Approved With Reservations

In my opinion, the results on differential distribution of histone modifications in sea and freshwater three-spined sticklebacks may potentially be interesting. Despite this, I strongly believe that text of the manuscript is currently beyond the minimal standards required for paper indexing.

Specifically: the abstract does not describe main findings of the paper in sufficient detail; the introduction does not provide an adequate background information for the study but, instead, mainly repeats the abstract; any Discussion comparing the results with already available literature is missing; some crucial details of the methodologies used (e.g. which antibodies have been used for CHIP) are missing from Methods; some sentences in the text are difficult to understand.

I recommend the authors to rewrite the text of manuscript addressing these points.

Competing Interests

No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Respond to this report

Responses (0)

[1] 1. Shlyueva D, Stampfel G, Stark A: Transcriptional enhancers: from properties to genome-wide predictions. Nat Rev Genet. 2014; 15(4): 272–286. PubMed Abstract | Publisher Full Text

[2] 2. Terekhanova NV, Logacheva MD, Penin AA, et al.: Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLoS Genet. 2014; 10(10): e1004696. PubMed Abstract | Publisher Full Text | Free Full Text

[3] 3. Filion GJ, Zhenilo S, Salozhin S, et al.: A family of human zinc finger proteins that bind methylated DNA and repress transcription. Mol Cell Biol. 2006; 26(1): 169–81. PubMed Abstract | Publisher Full Text | Free Full Text

[4] 4. Langmead B, Salzberg SL: Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9(4): 357–359. PubMed Abstract | Publisher Full Text | Free Full Text

[5] 5. Langmead B, Trapnell C, Pop M, et al.: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10(3): R25. PubMed Abstract | Publisher Full Text | Free Full Text

[6] 6. Zhang Y, Liu T, Meyer CA, et al.: Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008; 9(9): R137. PubMed Abstract | Publisher Full Text | Free Full Text

[7] 7. Quinlan AR, Hall IM: BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010; 26(6): 841–842. PubMed Abstract | Publisher Full Text | Free Full Text

[8] 8. Devireddy LR, Hart DO, Goetz DH, et al.: A mammalian siderophore synthesized by an enzyme with a bacterial homolog involved in enterobactin production. Cell. 2010; 141(6): 1006–17. PubMed Abstract | Publisher Full Text | Free Full Text

Analysis of distribution of chromatin marks across "divergence islands" in three-spined stickleback (Gasterosteus aculeatus)

Abstract

Keywords

Introduction

Methods

Sample preparation and ChIP experiment

Bioinformatics analysis

Results

Table 1. Results of reads mapping and peaks calling.

Table 2. Results of intersection of chromatin peaks with divergence islands and differential chromatin peaks analysis between MM and MF, and between FF and FM.

Table 3. Results of intersection of chromatin peaks with divergence islands and differential chromatin peaks analysis between FM and MM, and between MF and FF.

Conclusions

Data availability

Author contributions

Competing interests

Grant information

Acknowledgements

References

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