Abstract
Although a conserved SAGA complex containing the histone acetyltransferase GCN5 is known to mediate histone acetylation and transcriptional activation in eukaryotes, how to maintain different levels of histone acetylation and transcription at the whole-genome level remains to be determined. Here we identify and characterize a plant-specific GCN5-containing complex, which we term PAGA, in Arabidopsis thaliana and Oryza sativa. In Arabidopsis, the PAGA complex consists of two conserved subunits (GCN5 and ADA2A) and four plant-specific subunits (SPC, ING1, SDRL and EAF6). We find that PAGA and SAGA can independently mediate moderate and high levels of histone acetylation, respectively, thereby promoting transcriptional activation. Moreover, PAGA and SAGA can also repress gene transcription via the antagonistic effect between PAGA and SAGA. Unlike SAGA, which regulates multiple biological processes, PAGA is specifically involved in plant height and branch growth by regulating the transcription of hormone biosynthesis and response related genes. These results reveal how PAGA and SAGA cooperate to regulate histone acetylation, transcription and development. Given that the PAGA mutants show semi-dwarf and increased branching phenotypes without reduction in seed yield, the PAGA mutations could potentially be used for crop improvement.
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Data availability
A reporting summary for this paper is available as a Supplementary Information file. Raw RNA-seq and ChIP-seq data have been deposited in the Gene Expression Omnibus (GEO) database with the accession code GSE199761. The Arabidopsis and rice sequence data used in this study are from TAIR 10 and the CHINA RICE DATA CENTER, respectively. The accession numbers of genes reported in this study are as follows: GCN5 (AT3G54610), ADA2B (AT4G16420), ADA2A (AT3G07740), SPC (AT1G77800), ING1 (AT3G24010), SDRL (AT1G10310), EAF6 (AT4G14385), SGF29A (AT3G27460), SGF29B (AT5G40550), TAF5 (AT5G25150), TAF6 (AT1G04950), TAF6B (AT1G54360), TAF9 (AT1G54140), TAF10 (AT4G31720), TAF12 (AT3G10070), TAF12B (AT1G17440), SPT20 (AT1G72390), ADA1A (AT2G14850), ADA1B (AT4G33890), ADA1C (AT5G67410), ADA1D (AT4G31440), ADA1E (AT2G24530), TRA1A (AT2G17930), TRA1B (AT4G36080), SF3B3 (AT3G55200, AT3G55220), SF3B5A (AT3G23325), SF3B5B (AT4G14342), SCS1 (AT5G22450), SCS2A (AT2G19390), SCS2B (AT4G29790), TAFL (AT5G65540), HAM1 (AT5G64610), HAM2 (AT5G09740), EPL1A (AT1G16690), EPL1B (AT1G79020), EAF1A (AT3G24880), EAF1B (AT3G24870), ING2 (AT1G54390), SWC4 (AT2G47210), ARP4 (AT1G18450), EAF7 (AT1G26470), GAS41 (AT5G45600), MRG1 (AT4G37280), GA2OX2 (AT1G30040), GA2OX6 (AT1G02400), TCP15 (AT1G69690), IAA19 (AT3G15540), RAV2 (AT1G68840), MYB70 (AT2G23290), OsGCN5 (Os10g0415900), OsADA2 (Os03g0750800), OsSPCA (Os06g0209300), OsING1 (Os03g0143600), OsEAF6B (Os12g0298600), OsSDRL (Os02g0557700), OsTAF5A (Os06g0649500), OsTAF5B (Os07g0205200), OsTAF6 (Os01g0510800), OsTAF9A (Os03g0408500), OsTAF10 (Os09g0431500), OsTAF12B (Os01g0846900), OsSPT20 (Os10g0391100), OsADA1A (Os12g0580500), OsADA1B (Os03g0762700), OsSF3B3A (Os02g0137400), OsSF3B5A (Os08g0444100), OsSCS1A (Os01g0967100), OsSCS2 (Os05g0350700) and OsTAFL (Os03g0802300). Source data are provided with this paper.
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Acknowledgements
This work was supported by the National Natural Science Foundation of China (32025003) to X.-J.H.
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C.-J.W., Z.-Z.L., X.X., L.W., L.L. and S.C. performed the experiments. D.-Y.Y., X.-W.C. and Y.-N.S. performed the bioinformatics analyses. C.-J.W. and X.-J.H. designed the experiments and wrote the manuscript.
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Extended data
Extended Data Fig. 1 PAGA-dependent regulation of gene expression as determined by RNA-seq.
a, Scatter plots showing the correlation of gene expression changes between the spc mutant and the other PAGA mutants or the ada2b mutant. P values were generated by two-sided Pearson correlation test. b, Venn diagrams showing the overlap of down- and up-regulated DEGs (log2 FC > 1 or < −1, FDR < 0.05) in spc, spc ing1, and ada2a spc. P values were determined by the hypergeometric test (one-tailed). c, Heatmap showing the correlation of the effects of PAGA mutants on gene expression. Values indicate correlation coefficients.
Extended Data Fig. 2 Genome browser view of enriched signals of the ADA2B-, GCN5-, ADA2A-, and ING1-GFP proteins detected by ChIP-seq.
Screenshot showing some regions where both SAGA and PAGA are recruited and regions where only either SAGA or PAGA are recruited. Red boxes indicate SAGA- and PAGA-shared peaks. Pink boxes indicate SAGA-specific peaks. Green boxes indicate PAGA-specific peaks.
Extended Data Fig. 3 Identification of H3K9Ac and H3K14Ac level by ChIP-seq.
a, Genome browser view of H3K9Ac- and H3K14Ac-enriched peaks in WT detected by ChIP-seq. b, Percentage of genes with reduced (FC < 0.9, FDR < 0.01), increased (FC > 1.1, FDR < 0.01), and unchanged H3K14Ac levels in gcn5, ada2b, ada2a, and spc ing1 among the GCN5-, ADA2B-, ADA2A-, and ING1-bound genes, respectively. Values are the number of genes. c, Venn diagrams showing the overlap of ADA2B-, GCN5-, ADA2A-, and ING1-bound genes with reduced H3K14Ac level in ada2b, gcn5, ada2a, and spc ing1, respectively. d, Venn diagrams showing the overlap of H3K9Ac- and H3K14Ac-reduced target genes in ada2b, gcn5, ada2a, and spc ing1, respectively. e, Venn diagrams showing the overlap of H3K9Ac-reduced genes (FC < 0.9, FDR < 0.05) and expression-reduced genes (log2 FC < −1, FDR < 0.05) in gcn5, ada2b, ada2a, and spc ing1. P values were determined by the hypergeometric test (one-tailed).
Extended Data Fig. 4 H3K9Ac and H3K4me3 levels of SAGA- and PAGA-bound genes.
a, Boxplots showing the H3K9Ac and H3K4me3 levels of total SAGA- and PAGA-bound genes and bound genes with reduced or increased/unchanged H3K9Ac level in the corresponding SAGA and PAGA mutants. Random: 5000 random genes. Sample size of each boxplot: GCN5-bound a (n = 10081), b (n = 4717), and c (n = 5364); ADA2B-bound a (n = 6033), b (n = 3035), and c (n = 2998); ADA2A-bound a (n = 6940), b (n = 2234), and c (n = 4706); and ING1-bound a (n = 12989), b (n = 3095), c (n = 9894). In boxplots, centre lines and box edges are medians and the interquartile range (IQR), respectively. Whiskers extend within 1.5 times the IQR. P values determined by two-tailed Mann Whitney U test are indicated above boxes. b, H3K9Ac and H3K4me3 levels of SAGA- and PAGA-bound genes and of the bound genes with affected levels of H3K9Ac in the corresponding mutants. Total Arabidopsis genes were divided into deciles based on the H3K9Ac and H3K4me3 levels and sorted in ascending order. In each decile, the number of total ADA2B-, GCN5-, ADA2A-, and ING1-bound genes and of the bound genes with increased, reduced, and unchanged levels of H3K9Ac in the corresponding mutants are shown.
Extended Data Fig. 5 Morphological phenotypes of the SAGA and PAGA mutant plants.
a, Morphological phenotypes of the SAGA and PAGA mutant plants at different developmental stages. The top, middle, and bottom panels show 12-, 20-, and 31-day-old plants, respectively. b, The top panel shows images of trichomes on the adaxial side of the first leaf of WT, SAGA and PAGA mutant seedlings. Images are of 12-day-old seedlings grown on MS medium. The bottom panel shows morphological phenotypes of inflorescences in the SAGA and PAGA mutants. c, Left, shown are root length of 12-day-old seedlings (n = 20), numbers of the first rosette leaf with abaxial trichomes (n = 10), and numbers of rosette leaves from bolting plants (n = 24). ND indicates that ada2b mutant plants lacked trichomes on the abaxial side of rosette leaves. Right, shown are trichome numbers per leaf, leaf area, and trichome density on the adaxial side of the first leaf in the WT, SAGA and PAGA mutant seedlings (n = 10) (grown for 12 days on MS medium). Values are mean ± s.d. P values determined by two-tailed Student’s t-test are indicated above columns.
Extended Data Fig. 6 PAGA and SAGA antagonistically regulate plant development.
a, Morphological phenotypes of 30-day-old WT and T-DNA insertion mutant plants. b, Fresh weight of 30-day-old WT and T-DNA insertion mutant plants (n = 10). Values are mean ± s.d. P values determined by two-tailed Student’s t-test are indicated above columns.
Extended Data Fig. 7 Transcript levels of AT2G23290, AT2G17230, and AT1G70090 genes.
Transcript levels of indicated genes as determined RT-PCR. Values are means ± s.d. of three independent biological replicates. P values determined by two-tailed Student’s t-test are indicated above columns.
Supplementary information
Supplementary Information
Supplementary Figs. 1–15 and Tables 1 and 2.
Supplementary Data 1
Full list of co-purified proteins as determined by AP–MS using transgenic Arabidopsis plants in the WT and in the indicated mutant backgrounds.
Supplementary Data 2
Full list of co-purified proteins as determined by AP–MS using OsGCN5-GFP, OsADA2-GFP, OsSPCA-GFP and OsING1-GFP transgenic rice plants in the WT background.
Supplementary Data 3
Differentially expressed genes in the 12-day-old gcn5, ada2b, ada2a, spc, ing1, sdrl, eaf6, ada2a spc and spc ing1 mutants as determined by RNA-seq.
Supplementary Data 4
Peaks enriched by GCN5, ADA2B, ADA2A and ING1 as determined by ChIP-seq.
Supplementary Data 5
Peaks with reduced and increased H3K9Ac levels in the gcn5, ada2b, ada2a and spc ing1 mutants as determined by ChIP-seq.
Supplementary Data 6
Peaks with reduced and increased H3K14Ac levels in the gcn5, ada2b, ada2a and spc ing1 mutants as determined by ChIP-seq.
Supplementary Data 7
Differentially expressed genes in the 30-day-old gcn5, ada2b-c, ada2a, spc, ada2b-c ada2a and ada2b-c spc mutants as determined by RNA-seq.
Supplementary Data 8
List of primers used in this study.
Source data
Source Data Fig. 2
Unprocessed western blots.
Source Data Fig. 3
Unprocessed western blots.
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Wu, CJ., Yuan, DY., Liu, ZZ. et al. Conserved and plant-specific histone acetyltransferase complexes cooperate to regulate gene transcription and plant development. Nat. Plants 9, 442–459 (2023). https://doi.org/10.1038/s41477-023-01359-3
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DOI: https://doi.org/10.1038/s41477-023-01359-3
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