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

  1. Zhonghui Zhang
  2. Fuqu Hu
  3. Min Woo Sung
  4. Chang Shu
  5. Claudia Castillo-González
  6. Hisashi Koiwa
  7. Guiliang Tang
  8. Marty Dickman
  9. Pingwei Li  Is a corresponding author
  10. Xiuren Zhang  Is a corresponding author
  1. Texas A&M University, United States
  2. Michigan Technological University, United States

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).
    1. Min Woo Sung
    2. Pingwei Li
    3. and Xiuren Zhang
    (2017) protein structure of RICE1
    Publicly available at the RCSB Protein Data Bank (accession no. 5V5F).

Article and author information

Author details

  1. 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.
  2. 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.
  3. 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.
  4. 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.
  5. 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.
  6. Hisashi Koiwa

    Department of Horticulture, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Guiliang Tang

    Department of Biological Sciences, Michigan Technological University, Houghton, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6091-6921
  9. 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.
  10. 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.
    ORCID icon "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.

Reviewing Editor

  1. David Baulcombe, University of Cambridge, United Kingdom

Version history

  1. Received: December 21, 2016
  2. Accepted: April 29, 2017
  3. Accepted Manuscript published: May 2, 2017 (version 1)
  4. Version of Record published: May 31, 2017 (version 2)
  5. Version of Record updated: June 5, 2017 (version 3)

Copyright

© 2017, Zhang et al.

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.

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  1. Zhonghui Zhang
  2. Fuqu Hu
  3. Min Woo Sung
  4. Chang Shu
  5. Claudia Castillo-González
  6. Hisashi Koiwa
  7. Guiliang Tang
  8. Marty Dickman
  9. Pingwei Li
  10. Xiuren Zhang
(2017)
RISC-Interacting Clearing 3’- 5’ Exoribonucleases (RICEs) degrade uridylated cleavage fragments to maintain functional RISC in Arabidopsis
eLife 6:e24466.
https://doi.org/10.7554/eLife.24466

Share this article

https://doi.org/10.7554/eLife.24466

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