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Regulation of plant architecture by a new histone acetyltransferase targeting gene bodies

Nature Plants volume 6, pages 809–822 (2020)Cite this article

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Abstract

Axillary meristem development determines both plant architecture and crop yield; this critical process is regulated by the PROLIFERATING CELL FACTORS (TCP) family of transcription factors. Although TCP proteins bind primarily to promoter regions, some also target gene bodies for expression activation. However, the underlying regulatory mechanism remains unknown. Here we show that TEN, a TCP from cucumber (Cucumis sativus L.), controls the identity and mobility of tendrils. Through its C terminus, TEN binds at intragenic enhancers of target genes; its N-terminal domain functions as a non-canonical histone acetyltransferase (HAT) to preferentially act on lysine 56 and 122 of the histone H3 globular domain. This HAT activity is responsible for chromatin loosening and host-gene activation. The N termini of all tested CYCLOIDEA and TEOSINTE BRANCHED 1-like TCP proteins contain an intrinsically disordered region; despite their sequence divergence, they have conserved HAT activity. This study identifies a non-canonical class of HATs and provides a mechanism by which modification at the H3 globular domain is integrated with the transcription process.

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Fig. 1: Analysis of CRISPR–Cas9 mutants reveals the in vivo role of TEN.
Fig. 2: TEN is a transcription factor with intragenic binding capacity.
Fig. 3: TEN binds to intragenic enhancers of its target genes.
Fig. 4: TEN is a HAT.
Fig. 5: TEN promotes chromatin accessibility.
Fig. 6: The N termini of CYC/TB1-like proteins have conserved HAT activities.

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Data availability

The data supporting the findings in this study are available from the corresponding author upon reasonable request. Source data are provided with this paper.

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Acknowledgements

We thank Y. Huang and J. Doebley for comments on the manuscript, J. Lai, K. Liu, H. Deng, S. Fan, X. Chen, L. Guo and Y. Zhao for experimental assistance, and H. Wang for providing TB1 antibodies. This work was supported by National Key R&D Program of China (2019YFA0906200), the National Natural Science Foundation of China (31922076 to X.Y.) and the Central Public-Interest Scientific Institution Basal Research Fund (Y2017PT52). Additional support was provided by the Chinese Academy of Agricultural Science (ASTIP-CAAS, CAAS-XTCX2016001 and the Elite Young Scientists Program and The Agricultural Science and Technology Innovation Program), the Leading Talents of Guangdong Province Program (00201515 to S.H.), the Shenzhen Municipality (The Peacock Plan KQTD2016113010482651) and the Dapeng district government.

Author information

Author notes

  1. These authors contributed equally: Xueyong Yang, Jianbin Yan and Zhen Zhang.

Authors and Affiliations

  1. Key Laboratory of Biology and Genetic Improvement of Horticultural Crops of the Ministry of Agriculture, Sino-Dutch Joint Laboratory of Horticultural Genomics, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, China

    Xueyong Yang, Tongxu Xin & Zhonghua Zhang

  2. Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China

    Jianbin Yan, Tao Lin, Bowen Wang & Sanwen Huang

  3. College of Horticulture, Northwest A&F University, Yangling, China

    Zhen Zhang & Shenhao Wang

  4. State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China

    Zhen Zhang

  5. University of Chinese Academy of Sciences, National Laboratory of Biomacromolecules, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China

    Jicheng Zhao & Guohong Li

  6. Department of Plant Biology, College of Biological Sciences, University of California, Davis, CA, USA

    William J. Lucas

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Contributions

S.H. and X.Y. designed the research. X.Y., Zhen Zhang and B.W. made major contributions to biochemical analyses and ChIP assays. J.Y. contributed to protein purification. T.L., X.Y. and Zhonghua Zhang led bioinformatic analyses. X.Y. and T.X. led genetic transformation of plants. S.W. helped to collect tendril materials. G.L., J.Z. and Zhen Zhang contributed to histone purification and assembly. S.H., X.Y., G.L., W.J.L. and J.Y. analysed the data and wrote the manuscript.

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Correspondence to Sanwen Huang.

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Peer review information Nature Plants thanks Pilar Cubas, Richard Immink and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Identification of direct target genes of TEN and purification of the TEN truncated proteins.

a, Total protein extracts from tendrils or modified tendrils from WT, ten-1 and ten-2 plants were subjected to immunoblotting, using anti-TEN polyclonal antibody. The antibody recognized specifically a 50 KDa band (theoretical molar mass is approx. 45 KDa) in both WT and the ten-1 mutant, but not in the ten-2 null mutant. CBB, Coomassie Brilliant Blue staining. b, pCAMBIA 1300-c-Myc-TEN, and the corresponding vector, were transiently expressed in tobacco leaves. Total protein was extracted for immunoblotting, using anti-TEN and anti-c-Myc antibodies. Both antibodies recognized specifically the same bands at 70 KDa (5×c-Myc-tag peptide is 20 KDa). c, Total protein extracts from WT tendrils were subjected to immunoprecipitation with anti-TEN antibody. Input and immunoprecipitated protein fractions were analyzed by immunoblotting, using anti-TEN antibodies. SP, soluble protein; ISP, insoluble protein; IP-S, immunoprecipitation-supernatant fraction; W, wash fraction; P, pellet fraction; closed triangles indicate the target bands; asterisk, degradation of TEN protein. d, The TEN antibody recognized recombinant full-length TEN, but not its TCP domain. e, Schematic of the TEN binding peaks and target genes. f, Selected enrichment of GO terms for the 474 intragenic target genes. Significant analysis was done using a Fisher’s exact test. g, Exogenous treatment of ethephon promotes spontaneous tendril coiling. Spraying with water was carried out as control. h, Fragments Per Kilobase of exon per Million fragments mapped (FPKM) values of ACO1 gene in ten-1 different cucumber tissues, showing preferential expression in the tendril. i, Relative TEN expression levels, TEN binding levels to ACO1 and ACO1 expression levels during tendril growth (mean ± s.d, n = 3). The images in a-d and g were repeated at least twice, with similar results.

Source data

Extended Data Fig. 2 Purification of recombinant TEN and the TEN truncated proteins.

(a-c) Purification of MBP-TCP and MBP-TCP+R (a), FLAG-ΔN121 (b), and FLAG-TEN and FLAG-TENN338Y (c) proteins from transfected insect cells. The experiments were repeated at least three times, with similar results.

Source data

Extended Data Fig. 3 The binding specificity and affinity of the full length TEN to DNA containing the GGTCCC motif and the CTCCGCC motif identified by EMSA and SPR.

a, EMSA showing that TCP+R binds to a DNA probe containing the GGTCCC motif but does not bind to a DNA probe containing the CTCCGCC motif. b, EMSA showing binding of the TCP domain, to the GGTCCC motif, could not competed with the CTCCGCC motif. c and d, Surface plasmon resonance (SPR) curves for interactions of TCP+R with the DNA probes containing GGTCCC motif (c), or CTCCGCC motif (d). e, EMSA showing that full length TEN binds to a DNA probe containing the CTCCGCC motif and the GGTCCC motif. f and g, Surface plasmon resonance (SPR) curves for interactions of full length TEN with the DNA probes containing GGTCCC motif (f), or CTCCGCC motif (g). h, EMSA showing that the C terminus binding to the CTCCGCC motif could not be competed with the GGTCCC motif. i, The N338Y mutation, in the C-terminus of TEN, had no effect on TEN binding to the GGTCCC motif. j, Purification of MBP-tagged C-terminus of TEN. k, MBP-C protein could not bind to CTCCGCC probes. Comp, competitor (unlabeled probe); +/−, presence/absence of protein or competitor. The experiments were repeated twice, with similar results.

Source data

Extended Data Fig. 4 Functional validation for the importance of intragenic enhancer in ACO1 gene expression.

a, Expression of putative enhancer target gene, ERF1, and flanking genes, assayed by RT-qPCR (mean ± s.d, n = 3). UBQ was used as internal control. b, Schematic showing the design of synonymous mutations in the CTCCNCCN motifs for validation of ACO1 intragenic enhancers.

Extended Data Fig. 5 HAT activity of TEN demonstrated by LC-MS/MS analysis and immunoblotting assays.

a, PSI-BLAST analysis showing sequence similarity between N121 and the transferase domain within an Arabidopsis HXXXD acyltransferase, At1G03940. b, Purification of FLAG-N protein from insect cells; protein was identified by immunoblotting using anti-FLAG antibody. c–e, MS/MS spectrum of the charged ions corresponding to the H3 peptides where K56, K79 or K122 is acetylated. f-g, HAT assays of H3-H4 tetramer or nucleosome with FLAG-N121 (f) or FLAG-TEN proteins (g), followed by immunobloting with antibodies specific for different acetylated sites. h, Acetylation of different lysine sites, in histone H3, analyzed in tobacco leaves overexpressing c-Myc-TEN. Membrane blotted with H3K122ac was re-probed with anti-H3 to confirm equal loading. i- j, Overexpression of c-Myc-TEN promoted acetylation of chromatin-bound H3K56 (i) and K122 (j). Histone acetylation is shown in red (right), and nuclei transfected with c-Myc-TEN were visualized by FITC signal (green; middle). Nuclei were stained with DAPI (blue; left). Scale bar, 2 μm. The experiments in b-j were repeated at least 3 times, with similar results.

Source data

Extended Data Fig. 6 TEN promotes histone acetylation and chromatin accessibility at its gene targets.

a, Quantitative comparation of the histone acetyltransferase activity of N121 with a canonical HAT, CBP/P300, by quantitative mass spectrometry (mean ± s.d, n = 2). b, Metagene analysis showing genome-wide colocalization of TEN intragenic peaks with H3K56ac and H3K122ac in tendrils. c, d, Genomic browser tracks showing the TEN binding levels, H3K56ac levels, chromatin accessibility and mRNA expression at the TEN intragenic binding targets of ACO1 (c) and ERF1 (d).

Extended Data Fig. 7 Alignment of the IDRs of TB1-like proteins.

a, Alignment of the N-terminus of CYC/TB1-like proteins among selected angiosperm species, including Antirrhinum majus CYC, cucumber TEN, melon TEN, pumpkin TEN, watermelon TEN, soybean CYC, Durio CYC, grape CYC, Arabidopsis TCP1, cucumber BRC1, Arabidopsis BRC1, Arabidopsis BRC2, grape DICH, potato BRC1A, potato TCP7, sunflower TCP, rice TB1 and maize TB1. Red dashed boxes indicate the Gln14, Asp55 and Cys104 amino acid residues. b, Schematic of the different domains of four TB1-like proteins. Graphs plotting intrinsic disorder (PONDR VL3-BA) for selected TB1-like proteins. PONDR VL3-BA score (y-axis) and amino acid position (x-axis) are shown, indicating the intrinsically disordered and ordered regions.

Extended Data Fig. 8 HAT assays with mutant H3-H4 tetramer (H3K56R and H3K122R) by N121.

a, b, Acetylation of H3K56 and K122 within the wild type H3-H4 tetramer or mutant H3-H4 tetramer (H3K56R or H3K122R) by N121, determined by immunoblotting analysis. c, Acetylation of H3K56 and K122 within the wild type H3-H4 tetramer or mutant H3-H4 tetramer (H3K56R or H3K122R) by N121, determined by LC-MS/MS (mean ± s.d, n = 2). d–g, Acetylation of H3K56 and K122 within the wild type H3-H4 tetramer or mutant H3-H4 tetramer (H3K56R or H3K122R) by N terminus proteins of TEN, BRC1, BRC2 and durian CYC, determined by immunoblotting analysis. The representative images in a-b and d-g were repeated twice, with similar results.

Source data

Extended Data Fig. 9 Comparison of the regulatory datasets between TB1 and TEN.

All targets of TB1 and TEN could be classified within the categories including transcription factors, sugar metabolism, signal to stress, biosynthetic metabolism, phytohormone pathway or development. TEN target datasets did not show GO enrichment in light response, which was present in the GO results for the TB1 targets. HCBD, high confidence bound DEGs. Significance analysis was done using a Fisher’s exact test.

Extended Data Fig. 10 H3K56ac and H3K122ac are more likely to occur on exonic regions bound by TEN, HSF-1 and ERαc.

a, Distribution of binding peaks of enhancer-binding TFs, TEN, HSF-1 and ERα. b, Frequency of H3K56ac and/or H3K122ac on TEN, HSF-1 and ERα peaks, showing that histone globular acetylation is a general phenomenon for transcriptional regulation on exonic enhancers.

Supplementary information

Supplementary Information

Supplementary Figs. 1–5.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–9.

Supplementary Video 1

Time-lapse videos of wild-type and ten-3 mutant tendrils searching for a support and coiling. The wild-type tendrils could attach to a support, forming normal helical turns on each side of perversion. The mutant tendrils could still attach to a support, but the free coiling is impaired, causing reduced helical turns on both side of the perversion. The representative video was observed at least twice with similar results.

Supplementary Video 2

Time-lapse videos of wild-type and aco1-1 mutant tendrils searching for a support and coiling. The wild-type tendrils could attach to a support, forming normal helical turns on each side of perversion. The mutant tendrils form irregular coiling and could not attach to a support. The representative video was observed at least twice with similar results.

Source data

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Yang, X., Yan, J., Zhang, Z. et al. Regulation of plant architecture by a new histone acetyltransferase targeting gene bodies. Nat. Plants 6, 809–822 (2020). https://doi.org/10.1038/s41477-020-0715-2

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