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Proc Natl Acad Sci U S A. 2019 Dec 3;116(49):24542-24550. doi: 10.1073/pnas.1915312116. Epub 2019 Nov 21.

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

Author information

1
Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843.
2
School of Molecular Sciences, Arizona State University, Tempe, AZ 85287.
3
National Maize Improvement Center of China, China Agricultural University, 100193 Beijing, China.
4
College of Agronomy and Biotechnology, China Agricultural University, 100193 Beijing, China.
5
Center of Life Sciences, Skolkovo Institute of Science and Technology, 121205 Moscow, Russian Federation.
6
School of Molecular Sciences, Arizona State University, Tempe, AZ 85287; jlchen@asu.edu dshippen@tamu.edu.
7
Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843; jlchen@asu.edu dshippen@tamu.edu.

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.

KEYWORDS:

pseudoknot; reverse transcriptase; ribonucleoprotein; telomeres

PMID:
31754031
DOI:
10.1073/pnas.1915312116

Conflict of interest statement

The authors declare no competing interest.

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