Most cited article - PubMed ID 36546771
Telomerase RNA in Hymenoptera (Insecta) switched to plant/ciliate-like biogenesis
Telomeres, essential for maintaining genomic stability, are typically preserved through the action of telomerase, a ribonucleoprotein complex that synthesizes telomeric DNA. One of its two core components, telomerase RNA (TR), serves as the template for this synthesis, and its evolution across different species is both complex and diverse. This review discusses recent advancements in understanding TR evolution, with a focus on plants (Viridiplantae). Utilizing novel bioinformatic tools and accumulating genomic and transcriptomic data, combined with corresponding experimental validation, researchers have begun to unravel the intricate pathways of TR evolution and telomere maintenance mechanisms. Contrary to previous beliefs, a monophyletic origin of TR has been demonstrated first in land plants and subsequently across the broader phylogenetic megagroup Diaphoretickes. Conversely, the discovery of plant-type TRs in insects challenges assumptions about the monophyletic origin of TRs in animals, suggesting evolutionary innovations coinciding with arthropod divergence. The review also highlights key challenges in TR identification and provides examples of how these have been addressed. Overall, this work underscores the importance of expanding beyond model organisms to comprehend the full complexity of telomerase evolution, with potential applications in agriculture and biotechnology.
- Keywords
- TR evolution, TR identification, non-coding RNA, telomerase RNA, telomere,
- MeSH
- Phylogeny MeSH
- Evolution, Molecular * MeSH
- RNA, Plant * genetics MeSH
- RNA * genetics metabolism MeSH
- Plants * genetics MeSH
- Telomerase * genetics metabolism MeSH
- Telomere * genetics metabolism MeSH
- Viridiplantae * genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Names of Substances
- RNA, Plant * MeSH
- RNA * MeSH
- Telomerase * MeSH
- telomerase RNA MeSH Browser
Most eukaryotic organisms employ a telomerase complex for the maintenance of chromosome ends. The core of this complex is composed of telomerase reverse transcriptase (TERT) and telomerase RNA (TR) subunits. The TERT reverse transcriptase (RT) domain synthesises telomeric DNA using the TR template sequence. The other TERT domains contribute to this process in different ways. In particular, the TERT RNA-binding domain (TRBD) interacts with specific TR motif(s). Using a yeast 3-hybrid system, we show the critical role of Arabidopsis thaliana (At) TRBD and embryophyta-conserved KRxR motif in the unstructured linker preceding the TRBD domain for binding to the recently identified AtTR subunit. We also show the essential role of the predicted P4 stem and pseudoknot AtTR structures and provide evidence for the binding of AtTRBD to pseudoknot and KRxR motif stabilising interaction with the P4 stem structure. Our results thus provide the first insight into the core part of the plant telomerase complex.
- Keywords
- A.thaliana telomerase, AtTERT, AtTR, Protein-RNA interactions, Yeast three-hybrid,
- MeSH
- Arabidopsis * genetics enzymology MeSH
- Nucleic Acid Conformation MeSH
- Arabidopsis Proteins * genetics metabolism chemistry MeSH
- RNA, Plant genetics metabolism MeSH
- RNA metabolism genetics MeSH
- Two-Hybrid System Techniques MeSH
- Telomerase * genetics metabolism chemistry MeSH
- Protein Binding MeSH
- Publication type
- Journal Article MeSH
Studies on human telomeres have established that telomeres exert a significant influence on lifespan and health of organisms. However, recent research has indicated that the original idea that telomeres affect lifespan in a universal and central manner across all eukaryotic species is an oversimplification. Indeed, findings from a variety of animal species revealed that the role of telomere biology in aging is more subtle and intricate than previously recognized. Here, we show how telomere biology varies depending on the taxon. We also show how telomere biology corresponds to basic life history traits and affects the life table of a species and investments in growth, body size, reproduction, and lifespan; telomeres are hypothesized to shape evolutionary perspectives for species in an active but complex manner. Our evaluation is based on telomere biology data from many examples from throughout the animal kingdom that vary according to the degree of organismal complexity and life history strategies.
- Keywords
- Aging, Life history traits, Lifespan, Telomerase, Telomeres,
- MeSH
- Biological Evolution MeSH
- Longevity MeSH
- Humans MeSH
- Aging genetics MeSH
- Telomerase * genetics MeSH
- Telomere MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Names of Substances
- Telomerase * MeSH
Discoveries over the recent decade have demonstrated the unexpected diversity of telomere DNA motifs in nature. However, currently available resources, 'Telomerase database' and 'Plant rDNA database', contain just fragments of all relevant literature published over decades of telomere research as they have a different primary focus and limited updates. To fill this gap, we gathered data about telomere DNA sequences from a thorough literature screen as well as by analysing publicly available NGS data, and we created TeloBase (http://cfb.ceitec.muni.cz/telobase/) as a comprehensive database of information about telomere motif diversity. TeloBase is supplemented by internal taxonomy utilizing popular on-line taxonomic resources that enables in-house data filtration and graphical visualisation of telomere DNA evolutionary dynamics in the form of heat tree plots. TeloBase avoids overreliance on administrators for future data updates by having a simple form and community-curation system for application and approval, respectively, of new telomere sequences by users, which should ensure timeliness of the database and topicality. To demonstrate TeloBase utility, we examined telomere motif diversity in species from the fungal genus Aspergillus, and discovered (TTTATTAGGG)n sequence as a putative telomere motif in the plant family Chrysobalanaceae. This was bioinformatically confirmed by analysing template regions of identified telomerase RNAs.
- MeSH
- Databases, Genetic * MeSH
- Nucleotide Motifs MeSH
- Plants genetics MeSH
- Telomerase * genetics MeSH
- Telomere genetics metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Telomerase * MeSH
BACKGROUND: While web-based tools such as BLAST have made identifying conserved gene homologs appear easy, genes with variable sequences pose significant challenges. Functionally important noncoding RNAs (ncRNA) often show low sequence conservation due to genetic variations, including insertions and deletions. Rather than conserved sequences, these RNAs possess highly conserved structural features across a broad phylogenetic range. Such features can be identified using the covariance models approach, which combines sequence alignment with a secondary RNA structure consensus. However, running standard implementation of that approach (Infernal) requires advanced bioinformatics knowledge compared to user-friendly web services like BLAST. The issue is partially addressed by RNAcentral, which can be used to search for homologs across a broad range of ncRNA sequence collections from diverse organisms but not across the genome assemblies. RESULTS: Here, we present GERONIMO, which conducts evolutionary searches across hundreds of genomes in a fully automated way. It provides results extended with taxonomy context, as summary tables and visualizations, to facilitate analysis for user convenience. Additionally, GERONIMO supplements homologous sequences with genomic regions to analyze promoter motifs or gene collinearity, enhancing the validation of results. CONCLUSION: GERONIMO, built using Snakemake, has undergone extensive testing on hundreds of genomes, establishing itself as a valuable tool in the identification of ncRNA homologs across diverse taxonomic groups. Consequently, GERONIMO facilitates the investigation of the evolutionary patterns of functionally significant ncRNA players, whose understanding has previously been limited to individual organisms and close relatives.
- Keywords
- Snakemake, evolution, high-throughput pipeline, sequence homology searches,
- MeSH
- Algorithms * MeSH
- Phylogeny MeSH
- Genomics MeSH
- RNA, Untranslated genetics chemistry MeSH
- RNA * MeSH
- Sequence Alignment MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- RNA, Untranslated MeSH
- RNA * MeSH