Nejvíce citovaný článek - PubMed ID 24334955
Compromised telomere maintenance in hypomethylated Arabidopsis thaliana plants
Involvement of epigenetic mechanisms in the regulation of telomeres and transposable elements (TEs), genomic regions with the protective and potentially detrimental function, respectively, has been frequently studied. Here, we analyzed telomere lengths in Arabidopsis thaliana plants of Columbia, Landsberg erecta and Wassilevskija ecotypes exposed repeatedly to the hypomethylation drug zebularine during germination. Shorter telomeres were detected in plants growing from seedlings germinated in the presence of zebularine with a progression in telomeric phenotype across generations, relatively high inter-individual variability, and diverse responses among ecotypes. Interestingly, the extent of telomere shortening in zebularine Columbia and Wassilevskija plants corresponded to the transcriptional activation of TEs, suggesting a correlated response of these genomic elements to the zebularine treatment. Changes in lengths of telomeres and levels of TE transcripts in leaves were not always correlated with a hypomethylation of cytosines located in these regions, indicating a cytosine methylation-independent level of their regulation. These observations, including differences among ecotypes together with distinct dynamics of the reversal of the disruption of telomere homeostasis and TEs transcriptional activation, reflect a complex involvement of epigenetic processes in the regulation of crucial genomic regions. Our results further demonstrate the ability of plant cells to cope with these changes without a critical loss of the genome stability.
- Klíčová slova
- Arabidopsis thaliana, cytosine methylation, epigenetics, telomeres, transposable elements, zebularine,
- MeSH
- aktivace transkripce genetika MeSH
- Arabidopsis genetika metabolismus MeSH
- cytidin analogy a deriváty genetika MeSH
- cytosin metabolismus MeSH
- epigeneze genetická genetika MeSH
- homeostáza telomer genetika MeSH
- metylace DNA genetika MeSH
- rostlinné buňky metabolismus MeSH
- telomery genetika MeSH
- transpozibilní elementy DNA genetika MeSH
- zkracování telomer genetika MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- cytidin MeSH
- cytosin MeSH
- pyrimidin-2-one beta-ribofuranoside MeSH Prohlížeč
- transpozibilní elementy DNA MeSH
Parallel research on multiple model organisms shows that while some principles of telomere biology are conserved among all eukaryotic kingdoms, we also find some deviations that reflect different evolutionary paths and life strategies, which may have diversified after the establishment of telomerase as a primary mechanism for telomere maintenance. Much more than animals, plants have to cope with environmental stressors, including genotoxic factors, due to their sessile lifestyle. This is, in principle, made possible by an increased capacity and efficiency of the molecular systems ensuring maintenance of genome stability, as well as a higher tolerance to genome instability. Furthermore, plant ontogenesis differs from that of animals in which tissue differentiation and telomerase silencing occur during early embryonic development, and the "telomere clock" in somatic cells may act as a preventive measure against carcinogenesis. This does not happen in plants, where growth and ontogenesis occur through the serial division of apical meristems consisting of a small group of stem cells that generate a linear series of cells, which differentiate into an array of cell types that make a shoot and root. Flowers, as generative plant organs, initiate from the shoot apical meristem in mature plants which is incompatible with the human-like developmental telomere shortening. In this review, we discuss differences between human and plant telomere biology and the implications for aging, genome stability, and cell and organism survival. In particular, we provide a comprehensive comparative overview of telomere proteins acting in humans and in Arabidopsis thaliana model plant, and discuss distinct epigenetic features of telomeric chromatin in these species.
- Klíčová slova
- Arabidopsis, aging, chromatin, epigenetics, human, review, telomerase, telomere,
- MeSH
- chromatin metabolismus MeSH
- epigeneze genetická MeSH
- lidé MeSH
- rostliny metabolismus MeSH
- stárnutí buněk genetika MeSH
- telomerasa metabolismus MeSH
- telomery metabolismus MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- chromatin MeSH
- telomerasa MeSH
Standard pathways involved in the regulation of telomere stability do not contribute to gradual telomere elongation observed in the course of A. thaliana calli propagation. Genetic and epigenetic changes accompanying the culturing of plant cells have frequently been reported. Here we aimed to characterize the telomere homeostasis during long term callus propagation. While in Arabidopsis thaliana calli gradual telomere elongation was observed, telomeres were stable in Nicotiana tabacum and N. sylvestris cultures. Telomere elongation during callus propagation is thus not a general feature of plant cells. The long telomere phenotype in Arabidopsis calli was correlated neither with changes in telomerase activity nor with activation of alternative mechanisms of telomere elongation. The dynamics of telomere length changes was maintained in mutant calli with loss of function of important epigenetic modifiers but compromised in the presence of epigenetically active drug zebularine. To examine whether the cell culture-induced disruption of telomere homeostasis is associated with the modulated structure of chromosome ends, epigenetic properties of telomere chromatin were analysed. Albeit distinct changes in epigenetic modifications of telomere histones were observed, these were broadly stochastic. Our results show that contrary to animal cells, the structure and function of plant telomeres is not determined significantly by the epigenetic character of telomere chromatin. Set of differentially transcribed genes was identified in calli, but considering the known telomere- or telomerase-related functions of respective proteins, none of these changes per se was apparently related to the elongated telomere phenotype. Based on our data, we propose that the disruption in telomere homeostasis in Arabidopsis calli arises from the interplay of multiple factors, as a part of reprogramming of plant cells to long-term culture conditions.
- Klíčová slova
- Arabidopsis thaliana, Callus, Chromosome stability, Epigenetics, Regenerated plants, Telomere,
- MeSH
- Arabidopsis účinky léků genetika metabolismus MeSH
- chromatin genetika MeSH
- cytidin analogy a deriváty farmakologie MeSH
- druhová specificita MeSH
- ekotyp MeSH
- epigeneze genetická účinky léků MeSH
- histony metabolismus MeSH
- homeostáza telomer * účinky léků MeSH
- messenger RNA genetika metabolismus MeSH
- mutace genetika MeSH
- proteiny huseníčku metabolismus MeSH
- regenerace účinky léků MeSH
- rostlinné geny MeSH
- tabák genetika MeSH
- techniky tkáňových kultur * MeSH
- telomerasa metabolismus MeSH
- telomery metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- chromatin MeSH
- cytidin MeSH
- histony MeSH
- messenger RNA MeSH
- proteiny huseníčku MeSH
- pyrimidin-2-one beta-ribofuranoside MeSH Prohlížeč
- telomerasa MeSH
Epigenetic mechanisms are involved in regulation of crucial cellular processes in eukaryotic organisms. Data on the epigenetic features of plant telomeres and their epigenetic regulation were published mostly for Arabidopsis thaliana, in which the presence of interstitial telomeric repeats (ITRs) may interfere with genuine telomeres in most analyses. Here, we studied the epigenetic landscape and transcription of telomeres and ITRs in Nicotiana tabacum with long telomeres and no detectable ITRs, and in Ballantinia antipoda with large blocks of pericentromeric ITRs and relatively short telomeres. Chromatin of genuine telomeres displayed heterochromatic as well as euchromatic marks, while ITRs were just heterochromatic. Methylated cytosines were present at telomeres and ITRs, but showed a bias with more methylation toward distal telomere positions and different blocks of B. antipoda ITRs methylated to different levels. Telomeric transcripts TERRA (G-rich) and ARRET (C-rich) were identified in both plants and their levels varied among tissues with a maximum in blossoms. Plants with substantially different proportions of internally and terminally located telomeric repeats are instrumental in clarifying the chromatin status of telomeric repeats at distinct chromosome locations.
- Klíčová slova
- Ballantinia antipoda, DNA methylation, Nicotiana tabacum, chromatin, epigenetics, histone modifications, telomere,
- Publikační typ
- časopisecké články MeSH