Identification of the highly accumulated microRNA*s in Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa).

Plant microRNAs (miRNAs) are crucial for the regulation of gene expression, which is involved in almost all the important biological processes. In the cytoplasm, the miRNA strand is selectively incorporated into a specific Argonaute (AGO)-associated gene silencing complex, while the miRNA* is degraded rapidly. Thus, most miRNA*s were thought to be biologically meaningless. Interestingly, several recent reports in both plants and animals have shaken this notion. Many miRNA*s were demonstrated to possess regulatory roles in gene expression. However, the low accumulation levels of most miRNA*s raise the question whether the activities of this small RNA (sRNA) species are widespread in plants. Here, by using publicly available sRNA high-throughput sequencing data, we found that the accumulation levels of several miRNA*s could be much higher than those of their miRNA partners in certain organs, mutants and/or AGO-associated silencing complexes of both Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa). Based on target prediction and degradome sequencing data-based validation, some of these highly accumulated miRNA*s were indicated to possess cleavage-based potential regulatory role on certain targets. Besides, some interesting biological interpretations were obtained based on the accumulation patterns of the miRNA*s, the annotations of the target genes, and literature mining. Taken together, the expanded list of the highly accumulated miRNA*s along with their potential target genes discovered in this study further strengthened the current notion that certain members of the miRNA* species are biologically relevant, which needs further inspection.

[1]  Pamela J Green,et al.  Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome , 2009, Nature Protocols.

[2]  R. Lister,et al.  Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis , 2008, Cell.

[3]  S. Henikoff,et al.  Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription , 2007, Nature Genetics.

[4]  Jia Liu,et al.  The TIGR rice genome annotation resource: annotating the rice genome and creating resources for plant biologists , 2003, Nucleic Acids Res..

[5]  Yi Xing,et al.  The Bifunctional microRNA miR-9/miR-9* Regulates REST and CoREST and Is Downregulated in Huntington's Disease , 2008, The Journal of Neuroscience.

[6]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[7]  Jing Zhang,et al.  Differential expression of the microRNAs in superior and inferior spikelets in rice (Oryza sativa). , 2011, Journal of experimental botany.

[8]  Dennis B. Troup,et al.  NCBI GEO: archive for high-throughput functional genomic data , 2008, Nucleic Acids Res..

[9]  Xuemei Chen,et al.  Small RNAs and their roles in plant development. , 2009, Annual review of cell and developmental biology.

[10]  E. Sontheimer,et al.  Origins and Mechanisms of miRNAs and siRNAs , 2009, Cell.

[11]  Robert Giegerich,et al.  RNAshapes: an integrated RNA analysis package based on abstract shapes. , 2006, Bioinformatics.

[12]  Jason S. Cumbie,et al.  Genome-Wide Profiling and Analysis of Arabidopsis siRNAs , 2007, PLoS biology.

[13]  D. Bartel,et al.  MicroRNAS and their regulatory roles in plants. , 2006, Annual review of plant biology.

[14]  Songgang Li,et al.  High-Resolution Mapping of Epigenetic Modifications of the Rice Genome Uncovers Interplay between DNA Methylation, Histone Methylation, and Gene Expression[W] , 2008, The Plant Cell Online.

[15]  Yijun Qi,et al.  DNA methylation mediated by a microRNA pathway. , 2010, Molecular cell.

[16]  B. F. Vaniushin,et al.  [DNA methylation and epigenetics]. , 2006, Genetika.

[17]  I. K. Jordan,et al.  Dual coding of siRNAs and miRNAs by plant transposable elements. , 2008, RNA.

[18]  D. Bartel,et al.  Endogenous siRNA and miRNA Targets Identified by Sequencing of the Arabidopsis Degradome , 2008, Current Biology.

[19]  X. Dai,et al.  psRNATarget: a plant small RNA target analysis server. , 2011, Nucleic acids research.

[20]  Hsien-Da Huang,et al.  Arabidopsis Argonaute 2 regulates innate immunity via miRNA393(∗)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. , 2011, Molecular cell.

[21]  S. Luo,et al.  Global identification of microRNA–target RNA pairs by parallel analysis of RNA ends , 2008, Nature Biotechnology.

[22]  M. Pellegrini,et al.  Genome-wide High-Resolution Mapping and Functional Analysis of DNA Methylation in Arabidopsis , 2006, Cell.

[23]  Stijn van Dongen,et al.  miRBase: tools for microRNA genomics , 2007, Nucleic Acids Res..

[24]  D. Nettleton,et al.  The Arabidopsis MicroRNA396-GRF1/GRF3 Regulatory Module Acts as a Developmental Regulator in the Reprogramming of Root Cells during Cyst Nematode Infection1[W][OA] , 2012, Plant Physiology.

[25]  Z. Weng,et al.  Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. , 2010, RNA.

[26]  Doron Betel,et al.  Widespread regulatory activity of vertebrate microRNA* species. , 2011, RNA.

[27]  Ming Chen,et al.  Construction of MicroRNA- and MicroRNA*-mediated regulatory networks in plants , 2011, RNA biology.

[28]  J. Paszkowski,et al.  Gene silencing and DNA methylation processes. , 2001, Current opinion in plant biology.

[29]  Yun Zheng,et al.  Transcriptome-wide identification of microRNA targets in rice. , 2010, The Plant journal : for cell and molecular biology.

[30]  Cameron Johnson,et al.  CSRDB: a small RNA integrated database and browser resource for cereals , 2006, Nucleic Acids Res..

[31]  Fatih Ozsolak,et al.  RNA sequencing: advances, challenges and opportunities , 2011, Nature Reviews Genetics.

[32]  Ming Chen,et al.  Toward microRNA-mediated gene regulatory networks in plants , 2011, Briefings Bioinform..

[33]  O. Voinnet Origin, Biogenesis, and Activity of Plant MicroRNAs , 2009, Cell.

[34]  Wen Huang,et al.  The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant , 2001, Nucleic Acids Res..

[35]  Yuanji Zhang,et al.  miRU: an automated plant miRNA target prediction server , 2005, Nucleic Acids Res..

[36]  Vincent Moulton,et al.  Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. , 2010, The Plant journal : for cell and molecular biology.

[37]  P. May,et al.  Stars and Symbiosis: MicroRNA- and MicroRNA*-Mediated Transcript Cleavage Involved in Arbuscular Mycorrhizal Symbiosis1[W][OA] , 2011, Plant Physiology.

[38]  Kan Nobuta,et al.  Plant MPSS databases: signature-based transcriptional resources for analyses of mRNA and small RNA , 2005, Nucleic Acids Res..

[39]  Hong Duan,et al.  The regulatory activity of microRNA* species has substantial influence on microRNA and 3′ UTR evolution , 2008, Nature Structural &Molecular Biology.