Telomeres in Plants and Humans: Not So Different, Not So Similar

Abstract

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.

Composition and Function of Telomerase—A Polymerase Associated with the Origin of Eukaryotes

“…Whole-mount in situ hybridization detected TR transcripts in the primary root and lateral root apices of 3-week-old seedlings and in cultured cells, but in other tissue samples, using northern hybridization, no TR signal was found [20]. Levels of TR or TERT transcripts correlate strongly with the telomerase activities observed in various plant tissues [7,11].…”

“…In humans, telomerase activity is detected in all early developmental stages and increases progressively with advancing embryonic stages. After the completion of organogenesis in the human fetus, telomerase is expressed only in proliferating tissue-specific stem cells (e.g., bone marrow progenitor cells and neural stem cells), while telomerase activity in somatic cells is downregulated (reviewed in [7]). However, a tendency to repress telomerase in mammalian somatic tissues was described only for mammalian species of weight greater than 1 kg; e.g., laboratory mice have a constitutive telomerase.…”

“…Analogous to mammals, telomerase activity is suppressed in terminally differentiated tissues, e.g., mature leaves or stems. Active telomerase is detected in organs and tissues such as seedlings, shoot and root tips, young and middle-age leaves, flowers, and floral buds with proliferating meristematic cells [7,[9][10][11][12][13].…”

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

“…Telomeres, as chromatin structures, are natural targets for epigenetic modifications (Garcia‐Cao et al , ; Garcia‐Cao et al , ; Gonzalo et al , ; Gonzalo et al , ) and, according to widespread opinion, have been regarded as heterochromatic structures. In agreement with this, heterochromatin‐specific epigenetic marks were found to be associated with mammalian telomeres and involved in the maintenance of their homeostasis and proper functions (reviewed in Blasco, ; Prochazkova Schrumpfová et al , ). In recent years, this concept was questioned by studies demonstrating that human telomeres are not purely heterochromatic structures but also exhibit euchromatic features represented by high levels of euchromatin‐specific H4K20me and H3K27ac modifications (Cubiles et al , ).…”

“…Telomeres, nucleoprotein structures forming the ends of linear eukaryotic chromosomes, represent functionally essential regions. They are involved in the maintenance of integrity of the genome by distinguishing natural chromosome ends from double‐stranded DNA breaks, and form a barrier protecting coding sequences inside chromosomes from loss due to incomplete end‐replication (reviewed in Prochazkova Schrumpfová et al , ).…”