RISC-Interacting Clearing 3’- 5’ Exoribonucleases (RICEs) degrade uridylated cleavage fragments to maintain functional RISC in Arabidopsis

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Abstract

RNA-induced Silencing Complex (RISC) is composed of miRNAs and AGO proteins. AGOs use miRNAs as guides to slice target mRNAs to produce truncated 5' and 3' RNA fragments. The 5' cleaved RNA fragments are marked with uridylation for degradation. Here, we identified novel cofactors of Arabidopsis AGOs, named RICE1 and RICE2. RICE proteins specifically degraded single-strand (ss) RNAs in vitro; but neither miRNAs nor miRNA*s in vivo. RICE1 exhibited a DnaQ-like exonuclease fold and formed a homohexamer with the active sites located at the interfaces between RICE1 subunits. Notably, ectopic expression of catalytically-inactive RICE1 not only significantly reduced miRNA levels; but also increased 5' cleavage RISC fragments with extended uridine tails. We conclude that RICEs act to degrade uridylated 5’ products of AGO cleavage to maintain functional RISC. Our study also suggests a possible link between decay of cleaved target mRNAs and miRNA stability in RISC.

Data availability

The following data sets were generated

1. Zhang Z
2. Zhang X
(2017) small RNAs in RICE mutants
Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE96951).

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE96951
(2017) protein structure of RICE1
Publicly available at the RCSB Protein Data Bank (accession no. 5V5F).

https://www.rcsb.org/pdb/explore/explore.do?structureId=5V5F

Article and author information

Author details

Zhonghui Zhang

Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States

Competing interests
The authors declare that no competing interests exist.
Fuqu Hu

Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States

Competing interests
The authors declare that no competing interests exist.
Min Woo Sung

Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States

Competing interests
The authors declare that no competing interests exist.
Chang Shu

Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States

Competing interests
The authors declare that no competing interests exist.
Claudia Castillo-González

Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States

Competing interests
The authors declare that no competing interests exist.
Hisashi Koiwa

Department of Horticulture, Texas A&M University, College Station, United States

Competing interests
The authors declare that no competing interests exist.
Guiliang Tang

Department of Biological Sciences, Michigan Technological University, Houghton, United States

Competing interests
The authors declare that no competing interests exist.
Marty Dickman

Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6091-6921
Pingwei Li

Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States

For correspondence
pingwei@tamu.edu

Competing interests
The authors declare that no competing interests exist.
Xiuren Zhang

Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States

For correspondence
xiuren.zhang@tamu.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8982-2999

Funding

National Science Foundation (CAREER MCB-1253369)

Xiuren Zhang

Cancer Prevention and Research Institute of Texas (RP160822)

Xiuren Zhang

The authors declare that there was no funding for this work.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.