Two combinatorial patterns of telomere histone marks in plants with canonical and non‐canonical telomere repeats

Abstract

Telomeres, nucleoprotein structures at the ends of linear eukaryotic chromosomes, are crucial for the maintenance of genome integrity. In most plants, telomeres consist of conserved tandem repeat units comprising the TTTAGGG motif. Recently, non-canonical telomeres were described in several plants and plant taxons, including the carnivorous plant Genlisea hispidula (TTCAGG/TTTCAGG), the genus Cestrum (Solanaceae; TTTTTTAGGG), and plants from the Asparagales order with either a vertebrate-type telomere repeat TTAGGG or Allium genus-specific CTCGGTTATGGG repeat. We analyzed epigenetic modifications of telomeric histones in plants with canonical and non-canonical telomeres, and further in telomeric chromatin captured from leaves of Nicotiana benthamiana transiently transformed by telomere CRISPR-dCas9-eGFP, and of Arabidopsis thaliana stably transformed with TALE_telo C-33GFP. Two combinatorial patterns of telomeric histone modifications were identified: (i) an Arabidopsis-like pattern (A. thaliana, G. hispidula, Genlisea nigrocaulis, Allium cepa, Narcissus pseudonarcissus, Petunia hybrida, Solanum tuberosum, Solanum lycopersicum) with telomeric histones decorated predominantly by H3K9me2; (ii) a tobacco-like pattern (Nicotiana tabacum, N. benthamiana, C. elegans) with a strong H3K27me3 signal. Our data suggest that epigenetic modifications of plant telomere-associated histones are related neither to the sequence of the telomere motif nor to the lengths of the telomeres. Nor the phylogenetic position of the species plays the role; representatives of the Solanaceae family are included in both groups. As both patterns of histone marks are compatible with fully functional telomeres in respective plants, we conclude that the described specific differences in histone marks are not critical for telomere functions.

Histone H1 protects telomeric repeats from H3K27me3 invasion inArabidopsis

“…Owing to their repetitive nature (Fojtová and Fajkus, 2014; Majerová et al, 2014; Vaquero-Sedas et al, 2011, 2012; Vega-Vaquero et al, 2016), the chromatin composition and organization of plant telomeres has long remained enigmatic (Achrem et al, 2020; Dvořáčková et al, 2015). ChIP dot-blot analyses indicated a dominance of H3K9me2 over H3K27me3 histone marks but some of the Arabidopsis telomere regions also display euchromatic H3K4me2/3 marks (Adamusová et al, 2020; Grafi et al, 2007; Vaquero-Sedas et al, 2011). Here, combining ChIP-seq, ChIP dot-blot with telomeric probes and in situ immunolocalization showed that H1 moderates by 2-to-4 fold the accumulation of this mark on telomeres.…”

“…A role for H1 in telomere chromatin composition and sub-nuclear positioning Considering that telomeres display a continuum of perfect telobox motifs and a propensity to attract TRB proteins (Schrumpfová et al, 2014), we assessed whether these chromosome domains were, similar to ITRs, subject to H3K27me3 enrichment in 2h1 plants. Because the perfect continuum of terminal telomeric motifs is not suited for quantitative NGS analyses, we examined telomeric H3K27me3 using dot-blot hybridization of anti-H3K27me3 and anti-H3 ChIP DNA to radioactively labeled concatenated telomeric probes (Adamusová et al, 2020). This led to the estimation that telomeres display an average ~4-fold H3K27me3 enrichment in 2h1 as compared to WT plants, independent of any detectable change in nucleosome occupancy ( Figure 6A and S14).…”

The epigenetic regulation of centromeres and telomeres in plants and animals

“…The epigenetic nature of telomeres and subtelomeres remains controversial ( Vaquero-Sedas and Vega-Palas 2011 , Galati et al 2013 , Ichikawa et al 2015 , Adamusová et al 2019 ). In the classic model, animal and plant telomeres were interpreted as heterochromatic structures ( Kavi et al 2005 , Postepska-Igielska et al 2013 ).…”

“…Similar results were obtained in studies on plant telomeres. In Arabidopsis , heterochromatin modifications, such as H3K9me2 and H3K27me3, as well as euchromatin H3K4me3 modification have been reported ( Vrbsky et al 2010 , Majerová et al 2014 , Adamusová et al 2019 ). This occurrence of both heterochromatin and euchromatin modifications in the Arabidopsis telomere region was defined as the presence of an “intermediate” heterochromatin ( Vrbsky et al 2010 , Majerová et al 2014 ).…”

Looking At the Past and Heading to the Future: Meeting Summary of the 6th European Workshop on Plant Chromatin 2019 in Cologne, Germany

“…One of them corresponds to the Arabidopsis-like pattern, where telomere histones are marked predominantly with H3K9me2. The other one is the tobacco-like pattern marked predominantly with H3K27me3 (Adamusová et al, 2019).…”