Searching for the link between telomere length and life history traits in plants

Eukaryotic chromosomes are capped by telomeres, heterochromatic regions mainly constituted by non-coding repetitive sequences, and telomeric DNA-binding proteins. Telomeres contribute to genome stability by protecting their blunt-ended termini from degradation (Watson and Riha, 2011). As conventional DNA polymerase fails to replicate the 5′-ends of linear DNA molecules, telomere maintenance relies on the activity of telomerase–ribonucleoprotein complex that promotes the elongation of tandem repeats through the core catalytic subunit telomerase reverse transcriptase (TERT).

In humans, telomerase is active during embryogenesis but downregulated after birth, excluding specific cell types (e.g., stem cells and T-lymphocytes). As somatic cells lose a portion of telomeric DNA at each division, shortening of telomeres marks the onset of the aging process and deterioration of adult bodies. In plants, telomerase is also active in compartments containing highly dividing cells but downregulated in differentiated tissues and mature organs. Nevertheless, apical meristems form new structures throughout post-embryonic development and their indeterminate growth largely determines the plant lifespan (Figure 1). Therefore, telomere length is associated with cell division capacity in eukaryotes, indicating evolutionary conservation of the fundamentals of telomere biology. However, the impact of telomere length on lifespan varies between mammals and plants, reflecting differences in their developmental programs (Schrumpfová et al., 2019).

Figure 1.

Telomerase activity in humans and plants. Telomerase activity is high in prostate tissues and endometrium in adult human bodies and in apical meristems in adult plant bodies. Shortening of telomeres is detected in differentiated tissues in both human and plants. Telomerase activity marks aging in humans and influences life history traits in plants. Figure credit: M. Osnato.

In a new “Breakthrough Report,” Choi et al. (2021) investigated the possible link between natural variation in telomere length and life history traits in selected annual plants. First, the authors took advantage both of whole genome re-sequencing data from 1,001 accessions of Arabidopsis thaliana and direct measurement using a restriction fragment approach to analyze telomeric tandem repeats. GWAS mapping revealed an association between natural variation in telomere length and polymorphisms in seven genomic regions, including AtTERT. Furthermore, the comparison of telomere lengths with ecotype geographic distribution and several developmental traits uncovered negative correlations with latitude and traits related to flowering time at low ambient temperatures. These findings suggested that natural variation in telomere length across accessions might have a geographical basis and might account for specific adaptative strategies. In particular, telomere length is negatively associated with timing of the floral transition: ecotypes with longer telomeres flower earlier.

The authors also confirmed this negative correlation in rice (Oryza sativa) and maize (Zea mays) by analyzing whole-genome re-sequencing and flowering time data for these cereals. As an example, early flowering rice varieties of the temperate japonica group displayed higher telomere repeat copy number compared with rice varieties of the tropical japonica group. It should also be mentioned that anticipated heading date in rice cultivars adapted to temperate regions is associated with loss-of-function mutations in important floral repressors.

In flowering plants, the timing of the floral transition represents a key adaptive trait and is finely tuned by a complex gene regulatory network that integrates developmental and environmental signals. Although natural variation in telomere length accounts only for a small percentage of phenotypic variation in flowering time, it constitutes an additional level of regulation underlying this important life history trait.

Yet, the molecular mechanisms underpinning the fascinating link between telomeres and plant ecology are still unresolved. Indeed, the polymorphisms found in cereal accessions do not associate with genes previously involved in telomere maintenance. Still, Arabidopsis could be used in future studies to decipher the impact of telomere length on the activity of the shoot apical meristem at the floral transition. As supporting evidence, plants carrying mutations in AtTERT were previously used to uncover the essential role of telomere length in meristematic activity and stem cell renewal during root development (González-García et al., 2015).

Conflict of interest statement. None declared.