Distinct and Cooperative Activities of HESO1 and URT1 Nucleotidyl Transferases in MicroRNA Turnover in Arabidopsis

Bin Tu, Li Liu, Chi Xu, Jixian Zhai, Shengben Li, Miguel A. Lopez, Yuanyuan Zhao, Yu Yu, Vanitharani Ramachandran, Guodong Ren, Bin Yu, Shigui Li, Blake C. Meyers, Beixin Mo, Xuemei Chen

Research output: Contribution to journalArticle

44 Citations (Scopus)

Abstract

3’ uridylation is increasingly recognized as a conserved RNA modification process associated with RNA turnover in eukaryotes. 2’-O-methylation on the 3’ terminal ribose protects micro(mi)RNAs from 3’ truncation and 3’ uridylation in Arabidopsis. Previously, we identified HESO1 as the nucleotidyl transferase that uridylates most unmethylated miRNAs in vivo, but substantial 3’ tailing of miRNAs still remains in heso1 loss-of-function mutants. In this study, we found that among nine other potential nucleotidyl transferases, UTP:RNA URIDYLYLTRANSFERASE 1 (URT1) is the single most predominant nucleotidyl transferase that tails miRNAs. URT1 and HESO1 prefer substrates with different 3’ end nucleotides in vitro and act cooperatively to tail different forms of the same miRNAs in vivo. Moreover, both HESO1 and URT1 exhibit nucleotidyl transferase activity on AGO1-bound miRNAs. Although these enzymes are able to add long tails to AGO1-bound miRNAs, the tailed miRNAs remain associated with AGO1. Moreover, tailing of AGO1-bound miRNA165/6 drastically reduces the slicing activity of AGO1-miR165/6, suggesting that tailing reduces miRNA activity. However, monouridylation of miR171a by URT1 endows the miRNA the ability to trigger the biogenesis of secondary siRNAs. Therefore, 3’ tailing could affect the activities of miRNAs in addition to leading to miRNA degradation.

Original languageEnglish (US)
Article numbere1005119
JournalPLoS genetics
Volume11
Issue number4
DOIs
StatePublished - Apr 1 2015

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Transferases
MicroRNAs
microRNA
transferases
Arabidopsis
tailings
cooperatives
RNA
turnover
tail
slicing
ribose
methylation
eukaryote
eukaryotic cells
nucleotides
enzyme
substrate
mutants
degradation

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Distinct and Cooperative Activities of HESO1 and URT1 Nucleotidyl Transferases in MicroRNA Turnover in Arabidopsis. / Tu, Bin; Liu, Li; Xu, Chi; Zhai, Jixian; Li, Shengben; Lopez, Miguel A.; Zhao, Yuanyuan; Yu, Yu; Ramachandran, Vanitharani; Ren, Guodong; Yu, Bin; Li, Shigui; Meyers, Blake C.; Mo, Beixin; Chen, Xuemei.

In: PLoS genetics, Vol. 11, No. 4, e1005119, 01.04.2015.

Research output: Contribution to journalArticle

Tu, B, Liu, L, Xu, C, Zhai, J, Li, S, Lopez, MA, Zhao, Y, Yu, Y, Ramachandran, V, Ren, G, Yu, B, Li, S, Meyers, BC, Mo, B & Chen, X 2015, 'Distinct and Cooperative Activities of HESO1 and URT1 Nucleotidyl Transferases in MicroRNA Turnover in Arabidopsis', PLoS genetics, vol. 11, no. 4, e1005119. https://doi.org/10.1371/journal.pgen.1005119
Tu, Bin ; Liu, Li ; Xu, Chi ; Zhai, Jixian ; Li, Shengben ; Lopez, Miguel A. ; Zhao, Yuanyuan ; Yu, Yu ; Ramachandran, Vanitharani ; Ren, Guodong ; Yu, Bin ; Li, Shigui ; Meyers, Blake C. ; Mo, Beixin ; Chen, Xuemei. / Distinct and Cooperative Activities of HESO1 and URT1 Nucleotidyl Transferases in MicroRNA Turnover in Arabidopsis. In: PLoS genetics. 2015 ; Vol. 11, No. 4.
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