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-3×GFP. 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.

Department of Applied Biological Science Faculty of Science and Technology Tokyo University of Science 2641 Yamazaki Noda Chiba 278 8510 Japan

Laboratory of Functional Genomics and Proteomics National Centre for Biomolecular Research Faculty of Science Masaryk University 611 37 Brno Czech Republic

Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben 06466 Seeland Germany

Mendel Centre for Plant Genomics and Proteomics Central European Institute of Technology Masaryk University 625 00 Brno Czech Republic

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Arnoult, N., Van Beneden, A. and Decottignies, A. (2012) Telomere length regulates TERRA levels through increased trimethylation of telomeric H3K9 and HP1 alpha. Nat. Struct. Mol. Biol. 19, 948-956.

Blasco, M.A. (2007) The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 8, 299-309.

Bombarely, A., Moser, M., Amrad, A., Bao, M., Bapaume, L., Barry, C.S., Bliek, M., Boersma, M.R., Borghi, L. and Bruggmann, R. (2016) Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida. Nat. Plants, 2, 16074.

Cubiles, M.D., Barroso, S., Vaquero-Sedas, M.I., Enguix, A., Aguilera, A. and Vega-Palas, M.A. (2018) Epigenetic features of human telomeres. Nucleic Acids Res. 46, 2347-2355.

Cui, H., Zhang, S.T., Yang, H.J., Ji, H. and Wang, X.J. (2011) Gene expression profile analysis of tobacco leaf trichomes. BMC Plant Biol. 11, 76.

Dreissig, S., Schiml, S., Schindele, P., Weiss, O., Rutten, T., Schubert, V., Gladilin, E., Mette, M.F., Puchta, H. and Houben, A. (2017) Live-cell CRISPR imaging in plants reveals dynamic telomere movements. Plant J. 91, 565-573.

Dvořáčková, M., Fojtová, M. and Fajkus, J. (2015) Chromatin dynamics of plant telomeres and ribosomal genes. Plant J. 83, 18-37.

Fajkus, J., Kovarik, A., Kralovics, R. and Bezdek, M. (1995a) Organization of telomeric and subtelomeric chromatin in the higher plant Nicotiana tabacum. Mol. Gen. Genet. 247, 633-638.

Fajkus, J., Kralovics, R., Kovarik, A. and Fajkusova, L. (1995b) The telomeric sequence is directly attached to the HRS60 subtelomeric tandem repeat in tobacco chromosomes. FEBS Lett. 364, 33-35.

Fajkus, J., Novotna, M. and Ptacek, J. (2002) Analysis of chromosome termini in potato varieties. Rost Vyroba, 48, 477-479.

Fajkus, P., Peska, V., Sitova, Z., Fulneckova, J., Dvorackova, M., Gogela, R., Sykorova, E., Hapala, J. and Fajkus, J. (2016) Allium telomeres unmasked: the unusual telomeric sequence (CTCGGTTATGGG)nis synthesized by telomerase. Plant J. 85, 337-347.

Fojtová, M. and Fajkus, J. (2014) Epigenetic regulation of telomere maintenance. Cytogenet Genome Res. 143, 125-135.

Fojtová, M., Fajkus, P., Polanská, P. and Fajkus, J. (2015) Terminal restriction fragments (TRF) method to analyze telomere lengths. BIO-PROTOCOL, 5, e1671.

Fujimoto, S., Sugano, S.S., Kuwata, K., Osakabe, K. and Matsunaga, S. (2016) Visualization of specific repetitive genomic sequences with fluorescent TALEs in Arabidopsis thaliana. J. Exp. Bot. 67, 6101-6110.

Ganal, M.W., Lapitan, N.L.V. and Tanksley, S.D. (1991) Macrostructure of the tomato telomeres. Plant Cell, 3, 87-94.

Garcia-Cao, M., Gonzalo, S., Dean, D. and Blasco, M.A. (2002) A role for the Rb family of proteins in controlling telomere length. Nat. Genet. 32, 415-419.

Garcia-Cao, M., O'Sullivan, R., Peters, A.H.F.M., Jenuwein, T. and Blasco, M.A. (2004) Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat. Genet. 36, 94-99.

Gazzani, S., Gendall, A.R., Lister, C. and Dean, C. (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 132, 1107-1114.

Gonzalo, S., Garcia-Cao, M., Fraga, M.F. et al. (2005) Role of the RB1 family in stabilizing histone methylation at constitutive heterochromatin. Nat. Cell Biol. 7, 420-428.

Gonzalo, S., Jaco, I., Fraga, M.F., Chen, T.P., Li, E., Esteller, M. and Blasco, M.A. (2006) DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat. Cell Biol. 8, 416-424.

Greilhuber, J., Volleth, M. and Loidl, J. (1983) Genome size of man and animals relative to the plant Allium cepa. Can. J. Genet. Cytol. 25, 554-560.

He, L., Liu, J., Torres, G.A., Zhang, H.Q., Jiang, J.M. and Xie, C.H. (2013) Interstitial telomeric repeats are enriched in the centromeres of chromosomes in Solanum species. Chromosome Res. 21, 5-13.

Ijdo, J.W., Wells, R.A., Baldini, A. and Reeders, S.T. (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res. 19, 4780.

Leitch, I.J., Hanson, L., Lim, K.Y., Kovarik, A., Chase, M.W., Clarkson, J.J. and Leitch, A.R. (2008) The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Ann. Bot. 101, 805-814.

Majerova, E., Mandakova, T., Vu, G.T., Fajkus, J., Lysak, M.A. and Fojtova, M. (2014) Chromatin features of plant telomeric sequences at terminal vs. internal positions. Front. Plant Sci. 5, 593.

Mandakova, T., Joly, S., Krzywinski, M., Mummenhoff, K. and Lysak, M.A. (2010) Fast diploidization in close mesopolyploid relatives of Arabidopsis. Plant Cell, 22, 2277-2290.

Moyzis, R.K., Buckingham, J.M., Cram, L.S., Dani, M., Deaven, L.L., Jones, M.D., Meyne, J., Ratliff, R.L. and Wu, J.R. (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc. Natl Acad. Sci. USA, 85, 6622-6626.

Neplechova, K., Sykorova, E. and Fajkus, J. (2005) Comparison of different kinds of probes used for analysis of variant telomeric sequences. Biophys. Chem. 117, 225-231.

Ni, Z., Ng, D.W.-K., Liu, J. and Chen, Z.J. (2009) Chromatin immunoprecipitation (ChIP) assay. Protocol Exchange. https://doi.org/10.1038/nprot.2009.11

O'Sullivan, R.J., Kubicek, S., Schreiber, S.L. and Karlseder, J. (2010) Reduced histone biosynthesis and chromatin changes arising from a damage signal at telomeres. Nat. Struct. Mol. Biol. 17, 1218-1225.

Peska, V., Fajkus, P., Fojtova, M., Dvorackova, M., Hapala, J., Dvoracek, V., Polanska, P., Leitch, A.R., Sykorova, E. and Fajkus, J. (2015) Characterisation of an unusual telomere motif (TTTTTTAGGG)n in the plant Cestrum elegans (Solanaceae), a species with a large genome. Plant J. 82, 644-654.

Prochazkova Schrumpfova, P., Fojtova, M. and Fajkus, J. (2019) Telomeres in plants and humans: not so different, not so similar. Cells, 8, e58.

Richards, E.J. and Ausubel, F.M. (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell, 53, 127-136.

Rosenfeld, J.A., Wang, Z.B., Schones, D.E., Zhao, K., DeSalle, R. and Zhang, M.Q. (2009) Determination of enriched histone modifications in non-genic portions of the human genome. BMC Genom., 10, 143.

Schrumpfová, P.P., Fojtová, M. and Fajkus, J. (2019) Telomeres in plants and humans: not so different, not so similar. Cells, 8, 58.

Shakirov, E.V. and Shippen, D.E. (2004) Length regulation and dynamics of individual telomere tracts in wild-type Arabidopsis. Plant Cell, 16, 1959-1967.

Smykal, P., Gleissner, R., Corbesier, L., Apel, K. and Melzer, S. (2004) Modulation of flowering responses in different Nicotiana varieties. Plant Mol. Biol. 55, 253-262.

Sovakova, P.P., Magdolenova, A., Konecna, K., Rajecka, V., Fajkus, J. and Fojtova, M. (2018) Telomere elongation upon transfer to callus culture reflects the reprogramming of telomere stability control in Arabidopsis. Plant Mol. Biol. 98, 81-99.

Sykorova, E., Lim, K.Y., Kunicka, Z., Chase, M.W., Bennett, M.D., Fajkus, J. and Leitch, A.R. (2003a) Telomere variability in the monocotyledonous plant order Asparagales. Proc. Roy. Soc. B-Biol. Sci. 270, 1893-1904.

Sykorova, E., Lim, K.Y., Chase, M.W., Knapp, S., Leitch, I.J., Leitch, A.R. and Fajkus, J. (2003b) The absence of Arabidopsis-type telomeres in Cestrum and closely related genera Vestia and Sessea (Solanaceae): first evidence from eudicots. Plant J. 34, 283-291.

Sykorova, E., Leitch, A.R. and Fajkus, J. (2006) Asparagales telomerases which synthesize the human type of telomeres. Plant Mol. Biol. 60, 633-646.

The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.

The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature, 475, 189-195.

The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485, 635-641.

Tran, T.D., Cao, H.X., Jovtchev, G. et al. (2015) Centromere and telomere sequence alterations reflect the rapid genome evolution within the carnivorous plant genus Genlisea. Plant J. 84, 1087-1099.

Vaquero-Sedas, M.I., Gamez-Arjona, F.M. and Vega-Palas, M.A. (2011) Arabidopsis thaliana telomeres exhibit euchromatic features. Nucleic Acids Res. 39, 2007-2017.

Vaquero-Sedas, M.I., Luo, C.Y. and Vega-Palas, M.A. (2012) Analysis of the epigenetic status of telomeres by using ChIP-seq data. Nucleic Acids Res. 40.

Vrbsky, J., Akimcheva, S., Watson, J.M., Turner, T.L., Daxinger, L., Vyskot, B., Aufsatz, W. and Riha, K. (2010) siRNA-mediated methylation of Arabidopsis telomeres. PLoS Genet. 6, e1000986.

Vu, G.T.H., Schmutzer, T., Bull, F. et al. (2015) Comparative genome analysis reveals divergent genome size evolution in a carnivorous plant genus. Plant Genome, 8, 1-14.

Zonneveld, B.J.M. (2008) The systematic value of nuclear DNA content for all species of Narcissus L. (Amaryllidaceae). Plant Syst. Evol. 275, 109-132.

Chromosome engineering points to the cis-acting mechanism of chromosome arm-specific telomere length setting and robustness of plant phenotype, chromatin structure and gene expression

Optimizing ChIRP-MS for Comprehensive Profiling of RNA-Protein Interactions in Arabidopsis thaliana: A Telomerase RNA Case Study

Identification of the Sequence and the Length of Telomere DNA

Completing the TRB family: newly characterized members show ancient evolutionary origins and distinct localization, yet similar interactions

Polycomb Repressive Complex 2 in Eukaryotes-An Evolutionary Perspective

Distinct Responses of Arabidopsis Telomeres and Transposable Elements to Zebularine Exposure

Tidying-up the plant nuclear space: domains, functions, and dynamics