Contribution of the Histone Variant H2A.Z to Expression of Responsive Genes in Plants

Overview

Journal Semin Cell Dev Biol

Specialties Cell Biology
Reproductive Medicine

Date 2022 Apr 27

PMID 35474148

Authors

Jiaxin Long

Benjamin Carter

Emily T Johnson

Joe Ogas

Affiliations

Soon will be listed here.

Abstract

The histone variant H2A.Z plays a critical role in chromatin-based processes such as transcription, replication, and repair in eukaryotes. Although many H2A.Z-associated processes and features are conserved in plants and animals, a distinguishing feature of plant chromatin is the enrichment of H2A.Z in the bodies of genes that exhibit dynamic expression, particularly in response to differentiation and the environment. Recent work sheds new light on the plant machinery that enables dynamic changes in H2A.Z enrichment and identifies additional chromatin-based pathways that contribute to transcriptional properties of H2A.Z-enriched chromatin. In particular, analysis of a variety of responsive loci reveals a repressive role for H2A.Z in expression of responsive genes and identifies roles for SWR1 and INO80 chromatin remodelers in enabling dynamic regulation of H2A.Z levels and transcription. These studies lay the groundwork for understanding how this ancient histone variant is harnessed by plants to enable responsive and dynamic gene expression (Graphical Abstract).

Citing Articles

Characterizing the regulatory effects of H2A.Z and SWR1-C on gene expression during hydroxyurea exposure in Saccharomyces cerevisiae.

Brewis H, Stirling P, Kobor M PLoS Genet. 2025; 21(1):e1011566.

PMID: 39836664 PMC: 11761084. DOI: 10.1371/journal.pgen.1011566.

H2A.Z removal mediates the activation of genes accounting for cell elongation under light and temperature stress.

Do B, Nguyen N Plant Cell Rep. 2024; 43(12):286.

PMID: 39562374 DOI: 10.1007/s00299-024-03366-w.

Multifunctional histone variants in genome function.

Wong L, Tremethick D Nat Rev Genet. 2024; 26(2):82-104.

PMID: 39138293 DOI: 10.1038/s41576-024-00759-1.

Nematode histone H2A variant evolution reveals diverse histories of retention and loss and evidence for conserved core-like variant histone genes.

Singh S, Anderson N, Chu D, Roy S PLoS One. 2024; 19(5):e0300190.

PMID: 38814971 PMC: 11139335. DOI: 10.1371/journal.pone.0300190.

The master growth regulator DELLA binding to histone H2A is essential for DELLA-mediated global transcription regulation.

Huang X, Tian H, Park J, Oh D, Hu J, Zentella R Nat Plants. 2023; 9(8):1291-1305.

PMID: 37537399 PMC: 10681320. DOI: 10.1038/s41477-023-01477-y.

References

Osakabe A, Lorkovic Z, Kobayashi W, Tachiwana H, Yelagandula R, Kurumizaka H . Histone H2A variants confer specific properties to nucleosomes and impact on chromatin accessibility. Nucleic Acids Res. 2018; 46(15):7675-7685. PMC: 6125630. DOI: 10.1093/nar/gky540. View

Kumar S . H2A.Z at the Core of Transcriptional Regulation in Plants. Mol Plant. 2018; 11(9):1112-1114. DOI: 10.1016/j.molp.2018.07.002. View

Zahraeifard S, Foroozani M, Sepehri A, Oh D, Wang G, Mangu V . Rice H2A.Z negatively regulates genes responsive to nutrient starvation but promotes expression of key housekeeping genes. J Exp Bot. 2018; 69(20):4907-4919. PMC: 6137989. DOI: 10.1093/jxb/ery244. View

Peng M, Cui Y, Bi Y, Rothstein S . AtMBD9: a protein with a methyl-CpG-binding domain regulates flowering time and shoot branching in Arabidopsis. Plant J. 2006; 46(2):282-96. DOI: 10.1111/j.1365-313X.2006.02691.x. View

Lei B, Berger F . H2A Variants in : Versatile Regulators of Genome Activity. Plant Commun. 2021; 1(1):100015. PMC: 7747964. DOI: 10.1016/j.xplc.2019.100015. View

Carter B, Bishop B, Ho K, Huang R, Jia W, Zhang H . The Chromatin Remodelers PKL and PIE1 Act in an Epigenetic Pathway That Determines H3K27me3 Homeostasis in Arabidopsis. Plant Cell. 2018; 30(6):1337-1352. PMC: 6048792. DOI: 10.1105/tpc.17.00867. View

Bagchi D, Battenhouse A, Park D, Iyer V . The histone variant H2A.Z in yeast is almost exclusively incorporated into the +1 nucleosome in the direction of transcription. Nucleic Acids Res. 2019; 48(1):157-170. PMC: 7145542. DOI: 10.1093/nar/gkz1075. View

Zhang C, Cao L, Rong L, An Z, Zhou W, Ma J . The chromatin-remodeling factor AtINO80 plays crucial roles in genome stability maintenance and in plant development. Plant J. 2015; 82(4):655-68. DOI: 10.1111/tpj.12840. View

Weber C, Ramachandran S, Henikoff S . Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase. Mol Cell. 2014; 53(5):819-30. DOI: 10.1016/j.molcel.2014.02.014. View

10.

Ding J, Yu C, Sui Y, Wang L, Yang Y, Wang F . The chromatin remodeling protein INO80 contributes to the removal of H2A.Z at the p53-binding site of the p21 gene in response to doxorubicin. FEBS J. 2018; 285(17):3270-3285. DOI: 10.1111/febs.14615. View

11.

Molitor A, Bu Z, Yu Y, Shen W . Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet. 2014; 10(1):e1004091. PMC: 3900384. DOI: 10.1371/journal.pgen.1004091. View

12.

Talbert P, Ahmad K, Almouzni G, Ausio J, Berger F, Bhalla P . A unified phylogeny-based nomenclature for histone variants. Epigenetics Chromatin. 2012; 5:7. PMC: 3380720. DOI: 10.1186/1756-8935-5-7. View

13.

Luk E, Vu N, Patteson K, Mizuguchi G, Wu W, Ranjan A . Chz1, a nuclear chaperone for histone H2AZ. Mol Cell. 2007; 25(3):357-68. DOI: 10.1016/j.molcel.2006.12.015. View

14.

Subramanian V, Mazumder A, Surface L, Butty V, Fields P, Alwan A . H2A.Z acidic patch couples chromatin dynamics to regulation of gene expression programs during ESC differentiation. PLoS Genet. 2013; 9(8):e1003725. PMC: 3749939. DOI: 10.1371/journal.pgen.1003725. View

15.

Luo Y, Hou X, Zhang C, Tan L, Shao C, Lin R . A plant-specific SWR1 chromatin-remodeling complex couples histone H2A.Z deposition with nucleosome sliding. EMBO J. 2020; 39(7):e102008. PMC: 7110101. DOI: 10.15252/embj.2019102008. View

16.

Lazaro A, Gomez-Zambrano A, Lopez-Gonzalez L, Pineiro M, Jarillo J . Mutations in the Arabidopsis SWC6 gene, encoding a component of the SWR1 chromatin remodelling complex, accelerate flowering time and alter leaf and flower development. J Exp Bot. 2008; 59(3):653-66. DOI: 10.1093/jxb/erm332. View

17.

Berriri S, Gangappa S, Kumar S . SWR1 Chromatin-Remodeling Complex Subunits and H2A.Z Have Non-overlapping Functions in Immunity and Gene Regulation in Arabidopsis. Mol Plant. 2016; 9(7):1051-65. PMC: 4938710. DOI: 10.1016/j.molp.2016.04.003. View

18.

Wu W, Wu C, Ladurner A, Mizuguchi G, Wei D, Xiao H . N terminus of Swr1 binds to histone H2AZ and provides a platform for subunit assembly in the chromatin remodeling complex. J Biol Chem. 2008; 284(10):6200-7. PMC: 2649089. DOI: 10.1074/jbc.M808830200. View

19.

Yang C, Yin L, Xie F, Ma M, Huang S, Zeng Y . AtINO80 represses photomorphogenesis by modulating nucleosome density and H2A.Z incorporation in light-related genes. Proc Natl Acad Sci U S A. 2020; 117(52):33679-33688. PMC: 7777152. DOI: 10.1073/pnas.2001976117. View

20.

Dai X, Bai Y, Zhao L, Dou X, Liu Y, Wang L . H2A.Z Represses Gene Expression by Modulating Promoter Nucleosome Structure and Enhancer Histone Modifications in Arabidopsis. Mol Plant. 2017; 10(10):1274-1292. DOI: 10.1016/j.molp.2017.09.007. View