title: ARGONAUTE10 promotes the degradation of miR165/6 through the SDN1 and SDN2 exonucleases in Arabidopsis.
abstract: The degradation of small RNAs in plants and animals is associated with small RNA 3' truncation and 3' uridylation and thus relies on exonucleases and nucleotidyl transferases. ARGONAUTE (AGO) proteins associate with small RNAs in vivo and are essential for not only the activities but also the stability of small RNAs. AGO1 is the microRNA (miRNA) effector in Arabidopsis, and its closest homolog, AGO10, maintains stem cell homeostasis in meristems by sequestration of miR165/6, a conserved miRNA acting through AGO1. Here, we show that SMALL RNA DEGRADING NUCLEASES (SDNs) initiate miRNA degradation by acting on AGO1-bound miRNAs to cause their 3' truncation, and the truncated species are uridylated and degraded. We report that AGO10 reduces miR165/6 accumulation by enhancing its degradation by SDN1 and SDN2 in vivo. In vitro, AGO10-bound miR165/6 is more susceptible to SDN1-mediated 3' truncation than AGO1-bound miR165/6. Thus, AGO10 promotes the degradation of miR165/6, which is contrary to the stabilizing effect of AGO1. Our work identifies a class of exonucleases responsible for miRNA 3' truncation in vivo and uncovers a mechanism of specificity determination in miRNA turnover. This work, together with previous studies on AGO10, suggests that spatially regulated miRNA degradation underlies stem cell maintenance in plants.
authors.affiliation: Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California, Riverside, California, United States of America.
authors.forename: Yu
authors.initials: Y
authors.lastname: Yu
authors.affiliation: Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California, Riverside, California, United States of America.
authors.forename: Lijuan
authors.initials: L
authors.lastname: Ji
authors.affiliation: Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California, Riverside, California, United States of America.
authors.forename: Brandon H
authors.initials: BH
authors.lastname: Le
authors.affiliation: Department of Plant and Soil Sciences, and Delaware Biotechnology Institute, University of Delaware, Newark, Delaware, United States of America.
authors.forename: Jixian
authors.initials: J
authors.lastname: Zhai
authors.affiliation: Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California, Riverside, California, United States of America.|State Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and Development, Department of Biochemistry, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, China.
authors.forename: Jiayi
authors.initials: J
authors.lastname: Chen
authors.affiliation: Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California, Riverside, California, United States of America.
authors.forename: Elizabeth
authors.initials: E
authors.lastname: Luscher
authors.affiliation: Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California, Riverside, California, United States of America.
authors.forename: Lei
authors.initials: L
authors.lastname: Gao
authors.affiliation: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, West Lincui Road, Chaoyang District, Beijing, China.
authors.forename: Chunyan
authors.initials: C
authors.lastname: Liu
authors.affiliation: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, West Lincui Road, Chaoyang District, Beijing, China.
authors.forename: Xiaofeng
authors.initials: X
authors.lastname: Cao
authors.affiliation: Guangdong Provincial Key Laboratory for Plant Epigenetics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen, China.
authors.forename: Beixin
authors.initials: B
authors.lastname: Mo
authors.affiliation: State Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and Development, Department of Biochemistry, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, China.
authors.forename: Jinbiao
authors.initials: J
authors.lastname: Ma
authors.affiliation: Department of Plant and Soil Sciences, and Delaware Biotechnology Institute, University of Delaware, Newark, Delaware, United States of America.
authors.forename: Blake C
authors.initials: BC
authors.lastname: Meyers
authors.affiliation: Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California, Riverside, California, United States of America.|Howard Hughes Medical Institute, University of California, Riverside, California, United States of America.
authors.forename: Xuemei
authors.identifier: 0000-0002-5209-1157
authors.initials: X
authors.lastname: Chen
mesh_terms: D017360:Arabidopsis / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000378:metabolism*; D060565:Argonaute Proteins / Q000378:metabolism*; D005095:Exoribonucleases / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D008745:Methylation; D035683:MicroRNAs / Q000235:genetics / Q000378:metabolism*; D009154:Mutation / Q000235:genetics; D030821:Plants, Genetically Modified; D011485:Protein Binding; D020871:RNA Stability; D034743:RNA-Induced Silencing Complex / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D060565:Argonaute Proteins; D005095:Exoribonucleases; D035683:MicroRNAs; D034743:RNA-Induced Silencing Complex; C117457:AGO1 protein, Arabidopsis; C529694:AT5G43810 protein, Arabidopsis; C583141:MIRN165 microRNA, Arabidopsis; C580969:MIRN166 microRNA, Arabidopsis; C531524:SDN1 protein, Arabidopsis; C000620728:SDN2 protein, Arabidopsis