PEAT Complex and Plant H2A Deubiquitination

0
0
0

Title: The PEAT Complex Mediates Histone H2A Deubiquitination in Plants

Abstract

Histone post-translational modifications play a pivotal role in epigenetic regulation, influencing processes such as genome DNA replication, damage repair, and gene transcription. Histone H2A monoubiquitination (H2Aub) is highly conserved in plants and animals, often associated with gene repression. While the reversibility of histone ubiquitination is crucial for development, the molecular mechanisms underlying H2A deubiquitination in plants remain poorly understood. Here, we delve into the plant-specific PEAT complex and its role in H2A deubiquitination. This research uncovers that UBP5, a deubiquitinase, serves as a key player in plant H2A deubiquitination, and the PEAT complex’s modular components regulate H2Aub levels and H4K5 acetylation, providing insights into plant epigenetic regulation.

1. Introduction

Histone post-translational modifications, including methylation, acetylation, phosphorylation, and ubiquitination, are fundamental epigenetic regulators in eukaryotes. Histone H2A monoubiquitination (H2Aub) is conserved across plants and animals, typically linked to gene repression [1,2]. The reversibility of histone ubiquitination is vital for proper development, as imbalances can disrupt normal biological processes. In animals, E3 ligases forming the PRC1 complex catalyze H2Aub [1,3], but the deubiquitination machinery in plants is less characterized. Previous studies in Arabidopsis suggested that UBP12 and UBP13 are involved in H2A deubiquitination, yet they are not specific to H2A, highlighting the need to unveil plant-specific mechanisms.

2. The PEAT Complex and H2A Deubiquitination

The PEAT complex is a plant-specific multi-subunit complex identified in Arabidopsis, known to be involved in transposon silencing [10]. Recent research reveals that the PEAT complex interacts with UBP5, a deubiquitinase, and HAM1/2, histone acetyltransferases. In vitro assays using free histones and nucleosomes showed that UBP5 specifically deubiquitinates H2A on nucleosomes but not H2B, indicating its role in H2A deubiquitination [11]. Mutational analysis confirmed that UBP5 is crucial for regulating genome-wide H2Aub levels. For instance, in ubp5 mutants, H2Aub levels were significantly elevated, while H2Bub levels remained unaffected, underscoring UBP5’s specific role in H2A deubiquitination.

3. NuA4 Complex and H4K5 Acetylation

The NuA4 complex, highly conserved across eukaryotes, catalyzes histone acetylation. In Arabidopsis, HAM1/2 and EPL1A/1B form a functional equivalent of the NuA4 complex. The PEAT complex interacts with HAM1/2 via EPCR components, and this interaction is essential for H4K5 acetylation on nucleosomes [11]. Mutant studies showed that EPCR1/2 is necessary for H4K5 acetylation within the PEAT complex, linking acetylation to PEAT’s function in chromatin regulation.

4. PWWP Proteins in PEAT

PWWP proteins in the PEAT complex, such as PWWP1/2/3, interact with UBP5. Mutations in PWWP1/2 resulted in increased H2Aub levels, and ChIP-seq analysis confirmed that PWWP1/2 and UBP5 co-regulate H2Aub removal on thousands of target genes. Additionally, PEAT target genes exhibited lower H2Aub levels compared to other genes, establishing the UBP5-PWWP module as a key player in H2A deubiquitination.

5. Conclusion

The PEAT complex features two distinct modules: the UBP5-PWWP module responsible for H2A deubiquitination and the HAM1/2-EPCR module responsible for H4K5 acetylation. This dual functionality of the PEAT complex highlights its role in integrating chromatin regulation, providing a comprehensive understanding of plant epigenetic mechanisms. This work not only elucidates plant-specific H2A deubiquitination but also bridges the gap between histone ubiquitination and acetylation, paving the way for further studies on plant development and stress responses.

References

  1. Wang H, Wang L, Erdjument-Bromage H, et al. Role of histone H2A ubiquitination in polycomb silencing. Nature, 2004, 431: 873–878
  2. March E, Farrona S. Plant deubiquitinases and their role in the control of gene expression through modification of histones. Front Plant Sci, 2018, 8: 2274
  3. Cao R, Tsukada Y, Zhang Y. Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell, 2005, 20: 845–854
  4. Kralemann L E M, Liu S, Trejo-Arellano M S, et al. Removal of H2Aub1 by ubiquitin-specific proteases 12 and 13 is required for stable Polycomb-mediated gene repression in Arabidopsis. Genome Biol, 2020, 21: 144
  5. Derkacheva M, Liu S, Figueiredo D D, et al. H2A deubiquitinases UBP12/13 are part of the Arabidopsis polycomb group protein system. Nat Plants, 2016, 2: 16126
  6. Jeong J S, Jung C, Seo J S, et al. The deubiquitinating enzymes UBP12 and UBP13 positively regulate MYC2 levels in jasmonate responses. Plant Cell, 2017, 29: 1406–1424
  7. Lee C M, Li M W, Feke A, et al. GIGANTEA recruits the UBP12 and UBP13 deubiquitylases to regulate accumulation of the ZTL photoreceptor complex. Nat Commun, 2019, 10: 3750
  8. Liu G, Liang J, Lou L, et al. The deubiquitinases UBP12 and UBP13 integrate with the E3 ubiquitin ligase XBAT35.2 to modulate VPS23A stability in ABA signaling. Sci Adv, 2022, 8: eabl5765
  9. Xiong J, Yang F, Yao X, et al. The deubiquitinating enzymes UBP12 and UBP13 positively regulate recovery after carbon starvation by modulating BES1 stability in Arabidopsis thaliana. Plant Cell, 2022, 34: 4516–4530
  10. Tan L M, Zhang C J, Hou X M, et al. The PEAT protein complexes are required for histone deacetylation and heterochromatin silencing. EMBO J, 2018, 37: e98770
  11. Zheng S Y, Guan B B, Yuan D Y, et al. Dual roles of the Arabidopsis PEAT complex in histone H2A deubiquitination and H4K5 acetylation. Mol Plant, 2023, doi: 10.1016/j.molp.2023.10.006
  12. Doyon Y, Côté J. The highly conserved and multifunctional NuA4 HAT complex. Curr Opin Genet Dev, 2004, 14: 147–154
  13. Espinosa-Cores L, Bouza-Morcillo L, Barrero-Gil J, et al. Insights into the function of the NuA4 complex in plants. Front Plant Sci, 2020, 11: 125
  14. Barrero-Gil J, Bouza-Morcillo L, Espinosa-Cores L, et al. H4 acetylation by the NuA4 complex is required for plastid transcription and chloroplast biogenesis. Nat Plants, 2022, 8: 1052–1063
  15. Zhou J X, Su X M, Zheng S Y, et al. The Arabidopsis NuA4 histone acetyltransferase complex is required for chlorophyll biosynthesis and photosynthesis. J Integr Plant Biol, 2022, 64: 901–914
  16. Qin S, Min J. Structure and function of the nucleosome-binding PWWP domain. Trends Biochem Sci, 2014, 39: 536–547
  17. Hohenstatt M L, Mikulski P, Komarynets O, et al. PWWP-DOMAIN INTERACTOR OF POLYCOMBS1 interacts with polycomb-group proteins and histones and regulates arabidopsis flowering and development. Plant Cell, 2018, 30: 117–133
  18. Zhou J X, Liu Z W, Li Y Q, et al. Arabidopsis PWWP domain proteins mediate H3K27 trimethylation on FLC and regulate flowering time. J Integr Plant Biol, 2018, 60: 362–368
  19. Godwin J, March E, Govindasamy M, et al. The UBP5 histone H2A deubiquitinase counteracts PRC2-mediated repression to regulate Arabidopsis development and stress responses. bioRxiv, 2022, doi: 10.1101/2022.11.15.516593

DOI

doi: 10.1360/TB-2023-1063

Was this helpful?

0 / 0