Skip to main content
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian
  • Log in
  • My Cart

Main menu

  • Home
  • Articles
    • Current
    • Latest Articles
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • Archive
  • Front Matter
  • News
    • For the Press
    • Highlights from Latest Articles
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Purpose and Scope
    • Editorial and Journal Policies
    • Submission Procedures
    • For Reviewers
    • Author FAQ
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home

Advanced Search

  • Home
  • Articles
    • Current
    • Latest Articles
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • Archive
  • Front Matter
  • News
    • For the Press
    • Highlights from Latest Articles
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Purpose and Scope
    • Editorial and Journal Policies
    • Submission Procedures
    • For Reviewers
    • Author FAQ

New Research In

Physical Sciences

Featured Portals

  • Physics
  • Chemistry
  • Sustainability Science

Articles by Topic

  • Applied Mathematics
  • Applied Physical Sciences
  • Astronomy
  • Computer Sciences
  • Earth, Atmospheric, and Planetary Sciences
  • Engineering
  • Environmental Sciences
  • Mathematics
  • Statistics

Social Sciences

Featured Portals

  • Anthropology
  • Sustainability Science

Articles by Topic

  • Economic Sciences
  • Environmental Sciences
  • Political Sciences
  • Psychological and Cognitive Sciences
  • Social Sciences

Biological Sciences

Featured Portals

  • Sustainability Science

Articles by Topic

  • Agricultural Sciences
  • Anthropology
  • Applied Biological Sciences
  • Biochemistry
  • Biophysics and Computational Biology
  • Cell Biology
  • Developmental Biology
  • Ecology
  • Environmental Sciences
  • Evolution
  • Genetics
  • Immunology and Inflammation
  • Medical Sciences
  • Microbiology
  • Neuroscience
  • Pharmacology
  • Physiology
  • Plant Biology
  • Population Biology
  • Psychological and Cognitive Sciences
  • Sustainability Science
  • Systems Biology
Research Article

The conserved structure of plant telomerase RNA provides the missing link for an evolutionary pathway from ciliates to humans

View ORCID ProfileJiarui Song, Dhenugen Logeswaran, View ORCID ProfileClaudia Castillo-González, Yang Li, Sreyashree Bose, View ORCID ProfileBehailu Birhanu Aklilu, Zeyang Ma, Alexander Polkhovskiy, View ORCID ProfileJulian J.-L. Chen, and View ORCID ProfileDorothy E. Shippen
PNAS December 3, 2019 116 (49) 24542-24550; first published November 21, 2019 https://doi.org/10.1073/pnas.1915312116
Jiarui Song
aDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Jiarui Song
Dhenugen Logeswaran
bSchool of Molecular Sciences, Arizona State University, Tempe, AZ 85287;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Claudia Castillo-González
aDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Claudia Castillo-González
Yang Li
bSchool of Molecular Sciences, Arizona State University, Tempe, AZ 85287;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sreyashree Bose
aDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Behailu Birhanu Aklilu
aDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Behailu Birhanu Aklilu
Zeyang Ma
cNational Maize Improvement Center of China, China Agricultural University, 100193 Beijing, China;dCollege of Agronomy and Biotechnology, China Agricultural University, 100193 Beijing, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Alexander Polkhovskiy
aDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843;eCenter of Life Sciences, Skolkovo Institute of Science and Technology, 121205 Moscow, Russian Federation
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Julian J.-L. Chen
bSchool of Molecular Sciences, Arizona State University, Tempe, AZ 85287;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Julian J.-L. Chen
  • For correspondence: jlchen@asu.edu dshippen@tamu.edu
Dorothy E. Shippen
aDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Dorothy E. Shippen
  • For correspondence: jlchen@asu.edu dshippen@tamu.edu
  1. Edited by Thomas R. Cech, University of Colorado Boulder, Boulder, CO, and approved October 24, 2019 (received for review September 4, 2019)

  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

This article requires a subscription to view the full text. If you have a subscription you may use the login form below to view the article. Access to this article can also be purchased.

Significance

While telomerase has been extensively studied, its core RNA component (TR) is extremely divergent in sequence and biogenesis pathways, which has hindered our understanding of the evolutionary pathway from the small ciliate TR to the more complex fungal and vertebrate TRs. Here we report a conserved structure of the authentic TR from Arabidopsis thaliana termed AtTR, which is different from an RNA previously described as the templating telomerase RNA, AtTER1. This breakthrough establishes the correct A. thaliana TR and enables identification of TR homologs across the plant kingdom. Structural and functional analyses of AtTR reveals chimeric structural features similar to those of TRs from ciliates and multicellular eukaryotes, supporting the idea that all TRs are homologous, sharing a common ancestor.

Abstract

Telomerase is essential for maintaining telomere integrity. Although telomerase function is widely conserved, the integral telomerase RNA (TR) that provides a template for telomeric DNA synthesis has diverged dramatically. Nevertheless, TR molecules retain 2 highly conserved structural domains critical for catalysis: a template-proximal pseudoknot (PK) structure and a downstream stem-loop structure. Here we introduce the authentic TR from the plant Arabidopsis thaliana, called AtTR, identified through next-generation sequencing of RNAs copurifying with Arabidopsis TERT. This RNA is distinct from the RNA previously described as the templating telomerase RNA, AtTER1. AtTR is a 268-nt Pol III transcript necessary for telomere maintenance in vivo and sufficient with TERT to reconstitute telomerase activity in vitro. Bioinformatics analysis identified 85 AtTR orthologs from 3 major clades of plants: angiosperms, gymnosperms, and lycophytes. Through phylogenetic comparisons, a secondary structure model conserved among plant TRs was inferred and verified using in vitro and in vivo chemical probing. The conserved plant TR structure contains a template-PK core domain enclosed by a P1 stem and a 3′ long-stem P4/5/6, both of which resemble a corresponding structural element in ciliate and vertebrate TRs. However, the plant TR contains additional stems and linkers within the template-PK core, allowing for expansion of PK structure from the simple PK in the smaller ciliate TR during evolution. Thus, the plant TR provides an evolutionary bridge that unites the disparate structures of previously characterized TRs from ciliates and vertebrates.

  • ribonucleoprotein
  • reverse transcriptase
  • pseudoknot
  • telomeres

Footnotes

  • ↵1D.L. and C.C.-G. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: jlchen{at}asu.edu or dshippen{at}tamu.edu.
  • Author contributions: J.S., D.L., C.C.-G., Y.L., J.J.-L.C., and D.E.S. designed research; J.S., D.L., C.C.-G., Y.L., S.B., B.A., and A.P. performed research; J.S., D.L., C.C.-G., Y.L., Z.M., J.J.-L.C., and D.E.S. analyzed data; and J.S., D.L., C.C.-G., Y.L., J.J.-L.C., and D.E.S. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: Raw data from 2 independent RIP-seq and DMS-MaPseq experiments have been deposited in the Gene Expression Omnibus (GEO) database, https://www.ncbi.nlm.nih.gov/geo (BioProject ID PRJNA588284.). TRs identified in this work have been deposited in GenBank (accession no. TPA: BK011296–BK011375).

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1915312116/-/DCSupplemental.

Published under the PNAS license.

View Full Text

Log in using your username and password

Forgot your user name or password?

Purchase access

You may purchase access to this article. This will require you to create an account if you don't already have one.

Subscribers, for more details, please visit our Subscriptions FAQ.

Please click here to log into the PNAS submission website.

PreviousNext
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
The conserved structure of plant telomerase RNA provides the missing link for an evolutionary pathway from ciliates to humans
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
Citation Tools
The conserved structure of plant telomerase RNA provides the missing link for an evolutionary pathway from ciliates to humans
Jiarui Song, Dhenugen Logeswaran, Claudia Castillo-González, Yang Li, Sreyashree Bose, Behailu Birhanu Aklilu, Zeyang Ma, Alexander Polkhovskiy, Julian J.-L. Chen, Dorothy E. Shippen
Proceedings of the National Academy of Sciences Dec 2019, 116 (49) 24542-24550; DOI: 10.1073/pnas.1915312116

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
The conserved structure of plant telomerase RNA provides the missing link for an evolutionary pathway from ciliates to humans
Jiarui Song, Dhenugen Logeswaran, Claudia Castillo-González, Yang Li, Sreyashree Bose, Behailu Birhanu Aklilu, Zeyang Ma, Alexander Polkhovskiy, Julian J.-L. Chen, Dorothy E. Shippen
Proceedings of the National Academy of Sciences Dec 2019, 116 (49) 24542-24550; DOI: 10.1073/pnas.1915312116
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley
Proceedings of the National Academy of Sciences: 116 (50)
Current Issue

Submit

Sign up for Article Alerts

Article Classifications

  • Biological Sciences
  • Biochemistry

Jump to section

  • Article
    • Abstract
    • Results
    • Discussion
    • Materials and Methods
    • Acknowledgments
    • Footnotes
    • References
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Modulating the body's networks could become mainstream therapy for many health issues. Image credit: The Feinstein Institutes for Medicine Research.
Core Concept: The rise of bioelectric medicine sparks interest among researchers, patients, and industry
Modulating the body's networks could become mainstream therapy for many health issues.
Image credit: The Feinstein Institutes for Medicine Research.
Adaptations in heart structure and function likely enabled endurance and survival in preindustrial humans. Image courtesy of Pixabay/Skeeze.
Human heart evolved for endurance
Adaptations in heart structure and function likely enabled endurance and survival in preindustrial humans.
Image courtesy of Pixabay/Skeeze.
Viscoelastic carrier fluids enhance retention of fire retardants on wildfire-prone vegetation. Image courtesy of Jesse D. Acosta.
Viscoelastic fluids and wildfire prevention
Viscoelastic carrier fluids enhance retention of fire retardants on wildfire-prone vegetation.
Image courtesy of Jesse D. Acosta.
Water requirements may make desert bird declines more likely in a warming climate. Image courtesy of Sean Peterson (photographer).
Climate change and desert bird collapse
Water requirements may make desert bird declines more likely in a warming climate.
Image courtesy of Sean Peterson (photographer).
QnAs with NAS member and plant biologist Sheng Yang He. Image courtesy of Sheng Yang He.
Featured QnAs
QnAs with NAS member and plant biologist Sheng Yang He
Image courtesy of Sheng Yang He.

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Latest Articles
  • Archive

PNAS Portals

  • Classics
  • Front Matter
  • Teaching Resources
  • Anthropology
  • Chemistry
  • Physics
  • Sustainability Science

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Press
  • Site Map
  • PNAS Updates

Feedback    Privacy/Legal

Copyright © 2019 National Academy of Sciences. Online ISSN 1091-6490