The histone chaperones ASF1 and HIRA are required for telomere length and 45S rDNA copy number homeostasis

Plant J. 2024 Nov;120(3):1125-1141. doi: 10.1111/tpj.17041. Epub 2024 Oct 14.

Abstract

Genome stability is significantly influenced by the precise coordination of chromatin complexes that facilitate the loading and eviction of histones from chromatin during replication, transcription, and DNA repair processes. In this study, we investigate the role of the Arabidopsis H3 histone chaperones ANTI-SILENCING FUNCTION 1 (ASF1) and HISTONE REGULATOR A (HIRA) in the maintenance of telomeres and 45S rDNA loci, genomic sites that are particularly susceptible to changes in the chromatin structure. We find that both ASF1 and HIRA are essential for telomere length regulation, as telomeres are significantly shorter in asf1a1b and hira mutants. However, these shorter telomeres remain localized around the nucleolus and exhibit a comparable relative H3 occupancy to the wild type. In addition to regulating telomere length, ASF1 and HIRA contribute to silencing 45S rRNA genes and affect their copy number. Besides, ASF1 supports global heterochromatin maintenance. Our findings also indicate that ASF1 transiently binds to the TELOMERE REPEAT BINDING 1 protein and the N terminus of telomerase in vivo, suggesting a physical link between the ASF1 histone chaperone and the telomere maintenance machinery.

Keywords: 45S rDNA; ASF1; Arabidopsis thaliana; HIRA; chromatin; histone chaperones; telomeres.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • DNA, Ribosomal* / genetics
  • DNA, Ribosomal* / metabolism
  • Heterochromatin / genetics
  • Heterochromatin / metabolism
  • Histone Chaperones* / genetics
  • Histone Chaperones* / metabolism
  • Histones / genetics
  • Histones / metabolism
  • Molecular Chaperones / genetics
  • Molecular Chaperones / metabolism
  • RNA Splicing Factors
  • RNA, Ribosomal / genetics
  • RNA, Ribosomal / metabolism
  • Telomerase / genetics
  • Telomerase / metabolism
  • Telomere Homeostasis
  • Telomere* / genetics
  • Telomere* / metabolism

Substances

  • Arabidopsis Proteins
  • DNA, Ribosomal
  • Histone Chaperones
  • Cell Cycle Proteins
  • RNA, Ribosomal
  • Histones
  • RNA, ribosomal, 45S
  • Heterochromatin
  • Telomerase
  • Molecular Chaperones
  • At2g20020 protein, Arabidopsis
  • RNA Splicing Factors