Dynamics of H3K4me3 Chromatin Marks Prevails over H3K27me3 for Gene Regulation during Flower Morphogenesis in Arabidopsis thaliana
Abstract
:1. Introduction
2. Results
2.1. RNA-seq Reveals Specific Changes in Gene Expression during the Developmental Time Series
2.2. Meristem and Differentiated Tissues Share Similar Over-All Distribution of H3K27me3 and H3K4me3 Marks
2.3. H3K27me3 and H3K4me3 Levels are Highly Dynamic over the Time Series, in Accordance with Tissue Functionality
2.4. DMGs Largely Overlap with DEGs and Histone Mark Changes Are Stronger among DEGs
2.5. Expression Changes during Early Flower Morphogenesis Quantitatively Correlate with Changes in H3K4me3 While Changes in H3K27me3 Mostly Occur after Prolonged Expression Changes
2.6. Early Activation of PcG Target Genes is Mainly Accomponied by H3K4me3 Changes
2.7. Relative Dynamics of Histone Marks, MADS TF Binding and Chromatin Opening during Early Stages of Gene Activation
3. Discussion
3.1. Chromatin Marks are Highly Dynamic in Association with Tissue Fate during Flower Morphogenesis
3.2. Integrative Analysis of Chromatin and Expression Datasets Provides Insights on the Mechanistic of Gene Activation, Revealing Unexpected Order of Events
4. Materials and Methods
4.1. Plant Material and Growth Conditions
4.2. Dexamethasone Treatment and Harvesting of Plant Material
4.3. Scanning Electron Microscopy
4.4. Chromatin Immunoprecipitation
4.5. RNA Preparation, Reverse Transcription and Gene Expression Analysis by Semi-qPCR
4.6. Library Preparation and NGS
4.7. ChIP-seq Analysis
4.8. RNA-seq Analysis
4.9. Further Bioinformatics Analyses
4.9.1. Clustering
4.9.2. Gene Ontology Analysis
4.9.3. Visualisation of Data in a Genome Browser
4.9.4. Calculation of average histone mark abundance patterns and heat maps over a locus
4.9.5. Pearson Product-Moment Correlation Coefficient
4.10. Availability of Supporting Data
5. Conclusions
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
Abbreviations
AG | AGAMOUS |
AGL15 | AGAMOUS-Like 15 |
AIL6 | AINTEGUMENTA-LIKE 6 |
AP1-3 | APETALA 1-3 |
BXL1 | BETA-XYLOSIDASE 1 |
CAL | CAULIFLOWER |
ChIP | chromatin-immunoprecipitation |
CUP-SHAPED COTYLEDON 1 | CUC1 |
DEGs | differentially expressed genes |
DHS | DNase I hypersensitive |
DMGs | differentially marked genes |
EF1α | Elongation factor 1α |
FACS | fluorescence-activated cell sorting |
FLC | FLOWERING LOCUS C |
FT | FLOWERING LOCUS T |
GO | Gene Ontology |
IM | inflorescence meristem |
LAC10 | LACCASE 10 |
LBD39 | LOB DOMAIN-CONTAINING PROTEIN 39 |
LFY | LEAFY |
LSH | LIGHT SENSITIVE HYPOCOTYLS |
PcG | Polycomb Group |
PI | PISTILLATA |
PRCs | Polycomb repressive complexes |
PUP4 | PURINE PERMEASE 4 |
SAM | shoot apical meristem |
SDG4 | SET-DOMAIN-GROUP4 |
SEP1-4 | SEPALLATA 1-4 |
-seq | high-throughput sequencing |
SHP2 | SHATTERPROOF 2 |
SOC1 | SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 |
SPT | SPATULA |
SVP | SHORT VEGETATIVE PHASE |
TBP | TATA-box binding protein |
TF | transcription factor |
trxG | trithorax Group |
TSS | transcription start site |
UFO | UNUSUAL FLORAL ORGANS |
ULT1 | ULTRAPETALA 1 |
Appendix A. Additional Text
Appendix A.1. Description of Expression Clusters among Floral Regulator Genes
Appendix A.2. K-Means Clustering of DEGs
Appendix A.3. GO Analysis of DEGs
Appendix A.4. Quality Control for ChIP-seq Experiments
Appendix A.5. DMGs during Early Flower Morphogenesis
Appendix A.6. GO Analysis of DMGs
Appendix A.7. Analysis of DMGs That Are Not DEGs
Appendix B.
Appendix B.1. Supplementary Figure Legends
Appendix B.2. Supplementary Table Legends
References and Note
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Activation | ||||||
L < I | L < t0 | L < t2 | t0 < I | t2 < I | t0 < t2 | |
L < I | 4910 | |||||
L < t0 | 2835 | 4215 | ||||
L < t2 | 2832 | 3865 | 4246 | |||
t0 < I | 1496 | 154 | 181 | 3915 | ||
t2 < I | 1581 | 188 | 144 | 3252 | 4530 | |
t0 < t2 | 96 | 61 | 118 | 131 | 59 | 251 |
Repression | ||||||
L > I | L > t0 | L > t2 | t0 > I | t2 > I | t0 > t2 | |
L > I | 4629 | |||||
L > t0 | 3913 | 5683 | ||||
L > t2 | 3966 | 5170 | 5964 | |||
t0 > I | 186 | 65 | 98 | 1252 | ||
t2 > I | 145 | 54 | 40 | 930 | 1365 | |
t0 > t2 | 194 | 199 | 281 | 105 | 33 | 448 |
Activation | ||||
Identifier | Name | Domains/Family | Function | References |
At1g30840 | PURINE PERMEASE 4 (PUP4) | Member of a family of proteins related to PUP1, a purine transporter | putative purine transporter | [33] |
At1g45145 | LOCUS OF INSENSITIVITY TO VICTORIN 1 (LIV1), THIOREDOXIN H-TYPE 5 (TRX-H5) | cytosolic thioredoxin | response to biotic and abiotic stimuli | [34,35,36,37] |
At1g47610 | Transducin/WD40 repeat-like superfamily protein | unknown, known to be upregulated upon induction of AG function after 3 days | [38] | |
At1g75490 | DEHYDRATION-RESPONSIVE ELEMENT BINDING (DREB) A-2 ERF/AP2 TF family | DREB2A and DREB2B involved in drought response | [39,40] | |
At1g80110 | PHLOEM PROTEIN 2-B11 (PP2-B11) | putative carbohydrate binding | [41] | |
At3g02310 | SEPALLATA 2 (SEP2) | MADS TF | floral organ identity specification | [42,43] |
At4g32990 | Transducin/WD40 repeat-like superfamily | |||
At4g34230 | CINNAMYL ALCOHOL DEHYDROGENASE 5 (CAD5) | catalytically active cinnamyl alcohol dehydrogenase | [44] | |
At4g36930 | SPATULA (SPT) | bHLH TF | carpel development and seed dormancy regulation | [45,46] |
LACCASE 10 (LAC10) | putative laccase | [47] | ||
At5g10510 | AINTEGUMENTA-LIKE 6 (AIL6), PLETHORA 3 (PLT3) | AP2 domain TF | proliferation and differentiation in flowers, root stem cell identity, promote PIN1 expression and modulate local auxin production in phyllotaxis of the apex | [48,49] |
At5g15800 | SEPALLATA 1 (SEP1) | MADS TF | floral organ identity specification | [42,43] |
At5g61850 | LEAFY (LFY) | floral meristem identity control | [50,51,52] | |
Repression | ||||
Identifier | Name | Domains/Family | Function | References |
At1g05370 | Sec14p-like | phosphatidylinositol transfer | ||
At1g13260 | ETHYLENE RESPONSE DNA BINDING FACTOR 4 (EDF4), RELATED TO ABI3/VP11 (RAV1) | AP2/B3 domain TF | upregulated in low temperatures, has circadian regulation and may function as a negative growth regulator | [53,54] |
At1g13290 | DEFECTIVELY ORGANIZED TRIBUTARIES 5 (DOT5) WIP DOMAIN PROTEIN 6 (WIP6) | C2H2-ZF (type IIIA, subclass A1d) with a WIP domain. | venation in leaves, petiol development and phyllotaxy regulation | [55] |
At2g28550 | RELATED TO AP2.7 (RAP2.7), TARGET OF EARLY ACTIVATION TAGGED (EAT) 1 (TOE1) | AP2 TF | negative regulation of floral transition | [56] |
At2g31160 | LIGHT SENSITIVE HYPOCOTYLS 3 (LSH3), ORGAN BOUNDARY 1 (OBO1) | LSH1 family protein | may suppress organ differentiation in the boundary region of the SAM | [57,58,59] |
At2g34510 | unknown | expressed | ||
At3g04510 | LIGHT SENSITIVE HYPOCOTYLS 2 (LSH2) | LSH1 family | LHS1 regulates light regulation of seedling development | [57,58,59] |
At3g04520 | THREONINE ALDOLASE 2 (THA2) | threonine aldolase | threonine degradation to glycine | [60] |
At3g55240 | overexpression leads to Pseudo-Etiolation in Light | [61] | ||
At4g24110 | unknown | expressed, responds to karrikins | [62] | |
At4g37540 | LOB DOMAIN-CONTAINING PROTEIN 39 (LBD39) | LOB | downregulated in SET DOMAIN GROUP 4 mutant flowers (SDG4 maintain methylated histone H3 K4 and K36 levels) | [63] |
At5g06380 | expressed protein | unknown | ||
At5g28490 | LIGHT-DEPENDENT SHORT HYPOCOTYLS 1 (LSH1), ORGAN BOUNDARY 2 (OBO2) | LSH1 family | light regulation of seedling development in a phytochrome-dependent manner | [57,58,59] |
At5g44190 | GBF’S PRO-RICH REGION-INTERACTING FACTOR 2 (GPRI2), GOLDEN2-LIKE 2 (GLK2) | GOLDEN2-like TF | regulation of chloroplast development in a cell-autonomous manner, regulation of the expression of the photosynthetic apparatus, negative regulation of floral transition | [64] |
At5g49360 | BETA-XYLOSIDASE 1 (BXL1) | glycosyl hydrolase family 3 | β-D-xylosidase/α-L-arabinofuranosidase of the extracellular matrix required for pectic arabinan modification. expressed in tissues with secondary wall thickening, involved in seed germination | [65] |
PCC | Δ Normalised Read Count | ||||
---|---|---|---|---|---|
H3K27me3 | H3K4me3 | H3K27me3 | H3K4me3 | ||
up-regulated DEGs | t0-t2 | −0.104 | 0.456 | −0.004 | 0.139 |
t0-t2, K27 targets | −0.152 | 0.420 | −0.002 | 0.110 | |
t0-t2 & t0-I, K27 targets | −0.248 | 0.360 | −0.230 | 0.289 | |
down-regulated DEGs | t0-t2 | −0.012 | 0.420 | 0.032 | −0.190 |
t0-t2, K27 targets | −0.197 | 0.389 | 0.062 | −0.169 | |
t0-t2 & t0-I, K27 targets | −0.284 | 0.467 | 0.428 | −0.448 |
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Engelhorn, J.; Blanvillain, R.; Kröner, C.; Parrinello, H.; Rohmer, M.; Posé, D.; Ott, F.; Schmid, M.; Carles, C.C. Dynamics of H3K4me3 Chromatin Marks Prevails over H3K27me3 for Gene Regulation during Flower Morphogenesis in Arabidopsis thaliana. Epigenomes 2017, 1, 8. https://doi.org/10.3390/epigenomes1020008
Engelhorn J, Blanvillain R, Kröner C, Parrinello H, Rohmer M, Posé D, Ott F, Schmid M, Carles CC. Dynamics of H3K4me3 Chromatin Marks Prevails over H3K27me3 for Gene Regulation during Flower Morphogenesis in Arabidopsis thaliana. Epigenomes. 2017; 1(2):8. https://doi.org/10.3390/epigenomes1020008
Chicago/Turabian StyleEngelhorn, Julia, Robert Blanvillain, Christian Kröner, Hugues Parrinello, Marine Rohmer, David Posé, Felix Ott, Markus Schmid, and Cristel C. Carles. 2017. "Dynamics of H3K4me3 Chromatin Marks Prevails over H3K27me3 for Gene Regulation during Flower Morphogenesis in Arabidopsis thaliana" Epigenomes 1, no. 2: 8. https://doi.org/10.3390/epigenomes1020008