Year: 2023
Type: article
Abstract: One of the most fascinating phenomena in evolutionary biology is the rapid evolution of genes with conserved functions across the tree of life. Because cellular and organismal development processes are highly conserved across eukaryotes, a naive evolutionary expectation is that the genes involved in those processes would also be under high selective constraint and evolve extremely slowly. However, we now know that evolutionarily young genes can rapidly acquire crucial viability functions and even evolutionarily old genes can have unexpected levels of rapid evolution within specific lineages (Talbert et al., 2004). These studies have led to novel insights of function and evolution in molecular systems that are universally important for almost all organisms. The telomere is one such conserved molecular complex, but the adaptive evolutionary history of telomeres has received little attention. Telomeres are nucleoprotein complexes that cap chromosome ends for protection and proper elongation (Fulcher et al., 2014). Because of this vital function, one might expect the components of the telomere would be highly conserved and constrained from evolutionary change, which on the surface seems to be the case. For instance, 27 of the 29 protein subunits of the mammalian telomerase, a ribonucleoprotein enzyme that ensures the proper synthesis and maintenance of chromosome ends (Osterhage and Friedman, 2009) have a homolog in plants (Procházková Schrumpfová et al., 2019), indicating a common ancestral origin for the telomerase enzyme and deep evolutionary conservation. However, telomere protein sequences are highly divergent between species, and some of these evolutionary changes were fixed by adaptive evolution (Saint-Leandre and Levine, 2020). In addition, the noncoding RNA sequence that is crucial for the de novo synthesis of the telomeric repeats is extremely diverse in size, sequence, and structure (Podlevsky and Chen, 2016). What explains the rapid rate of sequence evolution but functional conservation for the molecular components of the telomere? In this perspective, we introduce the fascinating variation observed in plant telomeres. Rapidly developing genomic technology and the availability of abundant genomic data have revealed that plant telomeres are surprisingly variable compared to telomeres of other eukaryotic clades. We argue that understanding the biological basis of plant telomere variation is an important direction for future plant telomere research that will provide new insights on eukaryotic telomere function and evolution. All vertebrates have an identical telomere repeat sequence (TTAGGG)n (Meyne et al., 1989), indicating extreme purifying selection has prohibited evolutionary changes. But in plants, telomere sequences deviate from this ultraconstrained evolutionary history (Podlevsky and Chen, 2016; Shakirov et al., 2022). Arabidopsis thaliana was the first plant species to have its telomere sequence decoded (TTTAGGG)n, and subsequent studies revealed many plant species to also harbor the same Arabidopsis-type telomere sequence. But the sequence in multiple lineages deviates from the Arabidopsis-type sequence, and these sequences are categorized into two sequence-types (Peska and Garcia, 2020): (1) extension/contraction of thymine or guanine nucleotides [e.g., (TTTTTTAGGG)n in Cestrum elegans], and (2) insertion/substitution of non-(thymine/guanine) nucleotides [e.g., (TTCAGG)n and (TTTCAGG)n in the Genlisea group]. Extreme deviations, for instance, (CTCGGTTATGGG)n within the Allium group, display minimal resemblance to the Arabidopsis-type sequence. It is unclear what evolutionary pressure has driven the diversification of plant telomere sequences. One hypothesis is linked to the molecular activity of the telomerase. Telomerase comprises two main components, telomere reverse transcriptase (TERT) that synthesizes the telomere and telomerase RNA (TR), that acts as a template (Shakirov et al., 2022) (Figure 1). Alignment between the telomere DNA and TR is crucial for proper extension of the telomere, and the plant species that have diverged from the Arabidopsis-type telomere DNA sequence have also evolved the same changes in the TR template sequence (Fajkus et al., 2021). Why the TR sequence has evolved those changes is not known. Hints on the reason, however, can be gained from mammalian studies, where mutations in TR can influence the enzymatic activity of TERT (Chen and Greider, 2003). Whether the evolution of plant telomere sequences is linked to telomerase activity needs further study. Since telomere sequences are highly variable in plants, a natural question that arises is whether the proteins that bind to the telomere are also rapidly evolving. Very few studies in plants, however, have investigated the evolution of telomere-binding proteins. Protection of Telomeres 1 (POT1) is part of a nucleoprotein complex that binds and protects chromosome ends (de Lange, 2018). POT1 is a highly conserved telomere protein found in almost all eukaryotes, and interestingly, in plants the POT1 gene has duplicated multiple times (Beilstein et al., 2015). In A. thaliana, the POT1 paralogs are highly divergent (~50% amino acid similarity) from each other (Shakirov et al., 2005), and the divergence was partly driven by positive selection to enhance the binding of the POT1 paralog with other proteins that protect chromosome ends. (Beilstein et al., 2015). Importantly, investigating the evolution of the POT1 gene has led to a deeper understanding of telomere gene functions and the interaction among the molecular components of the telomere. Evolutionary analysis of telomere-binding proteins in animals have also revealed rapid evolution in several telomere genes (Saint-Leandre and Levine, 2020). What evolutionary driver could explain the rapid evolution of telomere-binding proteins in plants and animals? One hypothesis, the telomere conflict model (Saint-Leandre and Levine, 2020), postulates that the rapid evolution arose from an evolutionary arms race with subtelomeric transposable elements. Another model postulates that adaptation to biotic and abiotic stress is the evolutionary driver of telomere protein adaptive evolution (Shakirov et al., 2022). Many telomere proteins have pleiotropic roles, in particular for responding to oxidative stresses (Barnes et al., 2019), but the evolutionary link between the telomerase and stress response has not been tested. It is also possible that the telomere sequence and telomere-binding protein are subjected to the same evolutionary driver in plants and relates to the molecular activity of the telomerase. Clearly, we need to explore multiple models of telomere-binding protein evolution in plants, which we predict will uncover novel functions of telomerase. Misregulation of telomere length jeopardizes genomic stability and results in highly deleterious consequences for any organism. These deleterious fitness consequences might suggest telomere length would be under strong evolutionary and molecular constraints. However, telomere length varies significantly among species (e.g., A. thaliana telomere length is ~3 kbp while in tobacco 150 kbp) and even between individuals within the same species (e.g., A. thaliana ecotypes can differ up to 10-fold) (Shakirov et al., 2022). Quantitative genetics and functional validation studies have shown that plant telomere length variation is a heritable complex trait and controlled by natural genetic polymorphisms (Abdulkina et al., 2019). The highly variable telomere lengths in plants are intriguing, but also perplexing. What is the functional consequence of variable telomere lengths and is natural selection involved in shaping the length variation? A popular model explains variations in telomere length as an evolutionary outcome of life-history trade-offs (Young, 2018). In mammals, the association between lifespan and telomere length suggests telomere length has a role in aging and is subject to natural selection. But aging in plants differs fundamentally from that in mammals (Watson and Riha, 2011); hence, various models on the evolution of telomere length that are based on animal systems are not completely applicable for plants. In addition, several life-history traits differ fundamentally between plant and animals (e.g., the annual versus perennial life-history variation within the same species; Friedman, 2020), and the sessile nature of plants place the environment as a strong factor that controls many plant traits. Hence, how plant telomere lengths can vary across space and time, at the population-level, and at the tissue-specific level within and between individuals are all largely unanswered questions that could lead to a unique understanding of plant telomere biology. Clearly, we need to consider alternative models to explain telomere length variation for plants. Recently, links between telomere length and plant reproductive fitness and physiological traits have been discovered (Choi et al., 2021; Campitelli et al., 2022). Importantly, the studies have shown that variation in plant life-history strategies can potentially influence the evolution of the telomere through natural selection. Elucidating the molecular link between the telomere length and life-history should reveal novel insights into plant adaptation and life-history trait evolution. In this essay, we presented more questions than answers regarding plant telomeric variation, but also highlighted exciting research that could help us understand plant telomere evolution and function. The plant telomere biology field has a deep history of molecular and biochemical research (Shakirov et al., 2022). Combining this rich functional genetic knowledge of plant telomeres with evolutionary genetic approaches would provide a powerful method to understand the biology underlying the diversity of telomeric variation in plants. Importantly, understanding plant telomeres could have far-reaching relevance especially for understanding the evolution of all eukaryotic telomeres. J.Y.C. conceptualized the manuscript. S.K. and J.Y.C. wrote and revised the manuscript. We thank Pamela Diggle for her patience and giving us the opportunity to write this essay. We also thank the two reviewers for their feedback and efforts to improve the manuscript. We thank X (Twitter) users for suggestions on the title of this essay. We apologize to many of the authors whose work we could not cite in a short essay. This work was supported by grants from the National Science Foundation (IOS-2204729) and the National Institute of General Medical Sciences of the National Institutes of Health under Award Number P20 GM103418 to J.Y.C.
Source: American Journal of Botany
DOI: 10.1002/ajb2.16244
Authors: Surbhi Kumawat, Jae Young Choi
Institution: University of Kansas
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: bronze
OpenAlex ID: W4386919877