Histone methylation controls telomerase-independent telomere lengthening in cells undergoing dedifferentiation

Abstract

Cellular dedifferentiation underlies topical issues in biology such as regeneration and nuclear cloning and has common features in plants and animals. In plants, this process characterizes the transition of differentiated leaf cells to protoplasts (plant cells devoid of cell walls) and is accompanied by global chromatin reorganization associated with reprogramming of gene expression. A screen for mutants defective in proliferation and callus formation identified kyp-2-a mutant in the KRYPTONITE (KYP)/SUVH4 gene encoding a histone H3 lysine 9 (H3K9) methyltransferase. Analysis of telomere length revealed stochastic telomerase-independent lengthening of telomeres in wild type but not in kyp-2 protoplasts. In kyp-2 mutant, telomeric repeats were no longer associated with dimethylated H3K9. The Arabidopsis telomerase reverse transcriptase (tert) mutant displayed accelerated proliferation despite its short telomeres, though it also showed accelerated cell death. Microarray analysis uncovered several components of the ubiquitin proteolytic system, which are downregulated in kyp-2 compared to wild-type protoplasts. Thus, our results suggest that histone methylation activity is required for the establishment/maintenance of the dedifferentiated state and/or reentry into the cell cycle, at least partly, through activation of genes whose products are involved in the ubiquitin proteolytic pathway. In addition, our results illuminate the complexity of cellular dedifferentiation, particularly the occurrence of DNA recombination that can lead to genome instability.

Direct conversion of root primordium into shoot meristem relies on timing of stem cell niche development

“…In addition to morphological constraints, epigenetic factors might prevent the organ switch as the expression of plant genes involved in cell differentiation or totipotency depends in part on changes in the chromatin landscape (Berdasco et al, 2008;Grafi, 2004;Grafi et al, 2007;He et al, 2012;Ikeuchi et al, 2015;Koukalova et al, 2005;Lafos et al, 2011;Zhang et al, 2011). Our data confirmed that, together with additional regulators of shoot development (e.g.…”

Seed maturation in Arabidopsis thaliana is characterized by nuclear size reduction and increased chromatin condensation

“…Developmental phase transitions are generally characterized by a transient loosening of chromatin compaction (10)(11)(12)(13)(14)(15)(16). In contrast, we found increased chromatin compaction in the seed during the transition from embryo to seedling (Fig.…”

“…Accordingly, developmental changes in the plant are often accompanied by active modification of the chromatin structure (12). For example, chromatin compaction is loosened in protoplasts and before flowering (13)(14)(15), but increases during cell differentiation in maturing leaves and during seedling establishment (10,16).…”

Impact of nucleosome dynamics and histone modifications on cell proliferation during Arabidopsis development

“…The histone methyltransferase mutant kryptonite (kyp/suvh4), with reduced H3K9me2, fails to form calli structures, suggesting a role of H3K9 methylation in the dedifferentiation and/or proliferation stages (Figure 1). Moreover, this mutant does not present the telomere lengthening, normally associated with the dedifferentiation process (Grafi et al, 2007). Furthermore, there is evidence that a PcG complex is necessary for cellular reprogramming.…”