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.

Core Facility Bioinformatics CEITEC Masaryk University Brno CZ 62500 Czech Republic

Department of Biomedical Engineering Faculty of Electrical Engineering and Communication Brno University of Technology Brno 616 00 Czech Republic

Gregor Mendel Institute of Molecular Plant Biology Austrian Academy of Sciences Vienna Biocenter Vienna 1030 Austria

iGReD Université Clermont Auvergne CNRS INSERM BP 38 Clermont Ferrand 63001 France

Laboratory of Functional Genomics and Proteomics NCBR Faculty of Science Masaryk University Brno CZ 61137 Czech Republic

Mendel Centre for Plant Genomics and Proteomics CEITEC Masaryk University Brno CZ 62500 Czech Republic

Molecular Systems Biology Department of Functional and Evolutionary Ecology Faculty of Life Sciences University of Vienna Vienna 1030 Austria

Nantes Université CNRS US2B UMR 6286 Nantes F 44000 France

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