A Resource for Inactivation of MicroRNAs Using Short Tandem Target Mimic Technology in Model and Crop Plants

Ting Peng; Mengmeng Qiao; Haiping Liu; Sachin Teotia; Zhanhui Zhang; Yafan Zhao; Bobo Wang; Dongjie Zhao; Lina Shi; Cui Zhang; Brandon Le; Kestrel Rogers; Chathura Gunasekara; Haitang Duan; Yiyou Gu; Lei Tian; Jinfu Nie; Jian Qi; Fanrong Meng; Lan Huang; Qinghui Chen; Zhenlin Wang; Jinshan Tang; Xiaoqing Tang; Ting Lan; Xuemei Chen; Hairong Wei; Quanzhi Zhao; Guiliang Tang

doi:10.1016/j.molp.2018.09.003

A Resource for Inactivation of MicroRNAs Using Short Tandem Target Mimic Technology in Model and Crop Plants

Mol Plant. 2018 Nov 5;11(11):1400-1417. doi: 10.1016/j.molp.2018.09.003. Epub 2018 Sep 19.

Authors

Ting Peng¹, Mengmeng Qiao², Haiping Liu², Sachin Teotia³, Zhanhui Zhang³, Yafan Zhao⁴, Bobo Wang⁴, Dongjie Zhao², Lina Shi³, Cui Zhang⁵, Brandon Le⁵, Kestrel Rogers⁵, Chathura Gunasekara⁶, Haitang Duan⁷, Yiyou Gu², Lei Tian³, Jinfu Nie⁸, Jian Qi⁹, Fanrong Meng³, Lan Huang¹⁰, Qinghui Chen¹¹, Zhenlin Wang⁷, Jinshan Tang¹², Xiaoqing Tang², Ting Lan¹³, Xuemei Chen¹⁴, Hairong Wei¹⁵, Quanzhi Zhao¹⁶, Guiliang Tang¹⁷

Affiliations

¹ Collaborative Innovation Center of Henan Grain Crops, Henan Agricultural University, Zhengzhou 450002, China; Key Laboratory of Rice Biology in Henan Province, Henan Agricultural University, Zhengzhou 450002, China; Department of Biological Sciences, Life Science and Technology Institute, Michigan Technological University, Houghton, MI 49931, USA.
² Department of Biological Sciences, Life Science and Technology Institute, Michigan Technological University, Houghton, MI 49931, USA.
³ Collaborative Innovation Center of Henan Grain Crops, Henan Agricultural University, Zhengzhou 450002, China; Department of Biological Sciences, Life Science and Technology Institute, Michigan Technological University, Houghton, MI 49931, USA.
⁴ Collaborative Innovation Center of Henan Grain Crops, Henan Agricultural University, Zhengzhou 450002, China; Key Laboratory of Rice Biology in Henan Province, Henan Agricultural University, Zhengzhou 450002, China.
⁵ Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California, Riverside, CA 92521, USA.
⁶ School of Forest Resources and Environmental Science, Life Science and Technology Institute, Michigan Technological University, Houghton, MI 49931, USA.
⁷ Department of Computer Science, Michigan Technological University, Houghton, MI 49931, USA.
⁸ Anhui Province Key Laboratory of Medical Physics and Technology, Center of Medical Physics and Technology, Hefei Institutes of Physical Science, Chinese Academy of Sciences, Hefei, Anhui, China; Hefei Cancer Hospital, Chinese Academy of Sciences, Hefei, Anhui, China; Guangzhou Institute of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou, China.
⁹ Anhui Province Key Laboratory of Medical Physics and Technology, Center of Medical Physics and Technology, Hefei Institutes of Physical Science, Chinese Academy of Sciences, Hefei, Anhui, China; Hefei Cancer Hospital, Chinese Academy of Sciences, Hefei, Anhui, China.
¹⁰ College of Information and Electrical Engineering, China Agricultural University, Beijing 100083, China.
¹¹ Department of Biological Sciences, Life Science and Technology Institute, Michigan Technological University, Houghton, MI 49931, USA; Department of Kinesiology and Integrative Physiology, Life Science and Technology Instituted, Michigan Technological University, Houghton, MI 49931, USA.
¹² School of Technology, Michigan Technological University, Houghton, MI 49931, USA.
¹³ Guangdong Provincial Key Laboratory for Plant Epigenetics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, P.R. China.
¹⁴ Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California, Riverside, CA 92521, USA; Guangdong Provincial Key Laboratory for Plant Epigenetics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, P.R. China. Electronic address: xuemei.chen@ucr.edu.
¹⁵ School of Forest Resources and Environmental Science, Life Science and Technology Institute, Michigan Technological University, Houghton, MI 49931, USA; Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing 100083, P.R. China. Electronic address: hairong@mtu.edu.
¹⁶ Collaborative Innovation Center of Henan Grain Crops, Henan Agricultural University, Zhengzhou 450002, China; Key Laboratory of Rice Biology in Henan Province, Henan Agricultural University, Zhengzhou 450002, China. Electronic address: qzzhaoh@126.com.
¹⁷ Collaborative Innovation Center of Henan Grain Crops, Henan Agricultural University, Zhengzhou 450002, China; Department of Biological Sciences, Life Science and Technology Institute, Michigan Technological University, Houghton, MI 49931, USA; Guangdong Provincial Key Laboratory for Plant Epigenetics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, P.R. China; Key Laboratory of Plant Stress Biology, State Key Laboratory of Cotton Biology, School of Life Sciences, Henan University, Kaifeng 475004, China. Electronic address: gtang1@mtu.edu.

PMID: 30243763
DOI: 10.1016/j.molp.2018.09.003

Abstract

microRNAs (miRNAs) are endogenous small non-coding RNAs that bind to mRNAs and target them for cleavage and/or translational repression, leading to gene silencing. We previously developed short tandem target mimic (STTM) technology to deactivate endogenous miRNAs in Arabidopsis. Here, we created hundreds of STTMs that target both conserved and species-specific miRNAs in Arabidopsis, tomato, rice, and maize, providing a resource for the functional interrogation of miRNAs. We not only revealed the functions of several miRNAs in plant development, but also demonstrated that tissue-specific inactivation of a few miRNAs in rice leads to an increase in grain size without adversely affecting overall plant growth and development. RNA-seq and small RNA-seq analyses of STTM156/157 and STTM165/166 transgenic plants revealed the roles of these miRNAs in plant hormone biosynthesis and activation, secondary metabolism, and ion-channel activity-associated electrophysiology, demonstrating that STTM technology is an effective approach for studying miRNA functions. To facilitate the study and application of STTM transgenic plants and to provide a useful platform for storing and sharing of information about miRNA-regulated gene networks, we have established an online Genome Browser (https://blossom.ffr.mtu.edu/designindex2.php) to display the transcriptomic and miRNAomic changes in STTM-induced miRNA knockdown plants.

Keywords: Arabidopsis; RNA-seq; crop; miRNA; short tandem target mimic (STTM).

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Arabidopsis / genetics*
Gene Expression Regulation, Plant / genetics
Gene Silencing / physiology
MicroRNAs / genetics*
Oryza / genetics
Plants, Genetically Modified / genetics
RNA, Plant / genetics
Solanum lycopersicum / genetics
Zea mays / genetics

Substances

MicroRNAs
RNA, Plant

Abstract

Publication types

MeSH terms

Substances

Grants and funding