Regulation of Plant Architecture by a New Histone Acetyltransferase Targeting Gene Bodies

Overview

Journal Nat Plants

Specialties Biology
Genetics

Date 2020 Jul 16

PMID 32665652

Citations 11

Authors

Xueyong Yang

Jianbin Yan

Zhen Zhang

Tao Lin

Tongxu Xin

Bowen Wang

Shenhao Wang

Jicheng Zhao

Zhonghua Zhang

William J Lucas

Guohong Li

Sanwen Huang

Affiliations

Soon will be listed here.

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.

Citing Articles

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The GRAS transcription factor CsTL regulates tendril formation in cucumber.

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References

Martin-Trillo M, Cubas P . TCP genes: a family snapshot ten years later. Trends Plant Sci. 2009; 15(1):31-9. DOI: 10.1016/j.tplants.2009.11.003. View

Howarth D, Donoghue M . Phylogenetic analysis of the "ECE" (CYC/TB1) clade reveals duplications predating the core eudicots. Proc Natl Acad Sci U S A. 2006; 103(24):9101-6. PMC: 1482573. DOI: 10.1073/pnas.0602827103. View

Doebley J, Stec A, Hubbard L . The evolution of apical dominance in maize. Nature. 1997; 386(6624):485-8. DOI: 10.1038/386485a0. View

Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M . The OsTB1 gene negatively regulates lateral branching in rice. Plant J. 2003; 33(3):513-20. DOI: 10.1046/j.1365-313x.2003.01648.x. View

Aguilar-Martinez J, Poza-Carrion C, Cubas P . Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell. 2007; 19(2):458-72. PMC: 1867329. DOI: 10.1105/tpc.106.048934. View

Blackwood E, Kadonaga J . Going the distance: a current view of enhancer action. Science. 1998; 281(5373):60-3. DOI: 10.1126/science.281.5373.60. View

Kvon E, Kazmar T, Stampfel G, Yanez-Cuna J, Pagani M, Schernhuber K . Genome-scale functional characterization of Drosophila developmental enhancers in vivo. Nature. 2014; 512(7512):91-5. DOI: 10.1038/nature13395. View

Gillies S, Morrison S, Oi V, Tonegawa S . A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell. 1983; 33(3):717-28. DOI: 10.1016/0092-8674(83)90014-4. View

Hebbes T, Clayton A, Thorne A, Crane-Robinson C . Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken beta-globin chromosomal domain. EMBO J. 1994; 13(8):1823-30. PMC: 395022. DOI: 10.1002/j.1460-2075.1994.tb06451.x. View

10.

Hahn S . Phase Separation, Protein Disorder, and Enhancer Function. Cell. 2018; 175(7):1723-1725. DOI: 10.1016/j.cell.2018.11.034. View

11.

Li B, Carey M, Workman J . The role of chromatin during transcription. Cell. 2007; 128(4):707-19. DOI: 10.1016/j.cell.2007.01.015. View

12.

Liu C, Lu F, Cui X, Cao X . Histone methylation in higher plants. Annu Rev Plant Biol. 2010; 61:395-420. DOI: 10.1146/annurev.arplant.043008.091939. View

13.

Rajagopalan M, Balasubramanian S, Ioshikhes I, Ramaswamy A . Structural dynamics of nucleosome mediated by acetylations at H3K56 and H3K115,122. Eur Biophys J. 2016; 46(5):471-484. DOI: 10.1007/s00249-016-1191-5. View

14.

Suzuki Y, Horikoshi N, Kato D, Kurumizaka H . Crystal structure of the nucleosome containing histone H3 with crotonylated lysine 122. Biochem Biophys Res Commun. 2015; 469(3):483-9. DOI: 10.1016/j.bbrc.2015.12.041. View

15.

Tessarz P, Kouzarides T . Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol. 2014; 15(11):703-8. DOI: 10.1038/nrm3890. View

16.

Rufiange A, Jacques P, Bhat W, Robert F, Nourani A . Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell. 2007; 27(3):393-405. DOI: 10.1016/j.molcel.2007.07.011. View

17.

Tropberger P, Pott S, Keller C, Kamieniarz-Gdula K, Caron M, Richter F . Regulation of transcription through acetylation of H3K122 on the lateral surface of the histone octamer. Cell. 2013; 152(4):859-72. DOI: 10.1016/j.cell.2013.01.032. View

18.

Williams S, Truong D, Tyler J . Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc Natl Acad Sci U S A. 2008; 105(26):9000-5. PMC: 2449354. DOI: 10.1073/pnas.0800057105. View

19.

Chen C, Carson J, Feser J, Tamburini B, Zabaronick S, Linger J . Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell. 2008; 134(2):231-43. PMC: 2610811. DOI: 10.1016/j.cell.2008.06.035. View

20.

Driscoll R, Hudson A, Jackson S . Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science. 2007; 315(5812):649-52. PMC: 3334813. DOI: 10.1126/science.1135862. View