Construction of MicroRNA- and MicroRNA*-mediated regulatory networks in plants

The critical biological roles of microRNAs (miRNAs) have been well recognized. However, knowledge on the regulatory activities of miRNA*s is limited. Although several studies point to the capacity of this small RNA species to repress target genes in animals, few related analyses were performed in plants. Here, we set out to uncover the repressive effects of miRNA*s on their targets in both Arabidopsis and rice. Systemic identification of miRNA*s was performed through secondary structure-based prediction and expression level-based verification. The targets of the miRNA*s were predicted and further filtered based on degradome sequencing data, resulting in comprehensive miRNA*—target lists with high reliability. Comprehensive miRNA—target lists were also obtained. The phenomenon that one transcript was targeted by two or more miRNA(*)s was observed, which was defined as co-regulation. Finally, comprehensive miRNA- and miRNA*-mediated regulatory networks were constructed. Further investigation of some specific subnetworks implied the utility of these networks for biologists. This study could broaden the current understanding of miRNA-mediated regulation in plants.

[1]  Gregory J. Hannon,et al.  Sorting of Small RNAs into Arabidopsis Argonaute Complexes Is Directed by the 5′ Terminal Nucleotide , 2008, Cell.

[2]  E. K. Yoon,et al.  ‘Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells’ , 2006, Nucleic acids research.

[3]  Jonathan D. G. Jones,et al.  A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling , 2006, Science.

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

[5]  G. Coruzzi,et al.  Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana , 2010, Proceedings of the National Academy of Sciences.

[6]  Yukihisa Shimada,et al.  GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. , 2006, The Plant journal : for cell and molecular biology.

[7]  Xuemei Chen,et al.  A MicroRNA as a Translational Repressor of APETALA2 in Arabidopsis Flower Development , 2004, Science.

[8]  K. D. Kasschau,et al.  A MicroRNA as a Translational Repressor of APETALA 2 in Arabidopsis Flower Development , 2022 .

[9]  J. Zethof,et al.  A conserved microRNA module exerts homeotic control over Petunia hybrida and Antirrhinum majus floral organ identity , 2007, Nature Genetics.

[10]  M. Crespi,et al.  miR390, Arabidopsis TAS3 tasiRNAs, and Their AUXIN RESPONSE FACTOR Targets Define an Autoregulatory Network Quantitatively Regulating Lateral Root Growth[W] , 2010, Plant Cell.

[11]  Elliot M Meyerowitz,et al.  Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness , 2007, Development.

[12]  W. Filipowicz,et al.  The widespread regulation of microRNA biogenesis, function and decay , 2010, Nature Reviews Genetics.

[13]  N. Chua,et al.  MicroRNA Directs mRNA Cleavage of the Transcription Factor NAC1 to Downregulate Auxin Signals for Arabidopsis Lateral Root Development , 2005, The Plant Cell Online.

[14]  E. Lai,et al.  Distinct mechanisms for microRNA strand selection by Drosophila Argonautes. , 2009, Molecular cell.

[15]  Gi-Ho Sung,et al.  Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana , 2004, Nature Genetics.

[16]  Ping Wu,et al.  High-throughput degradome sequencing can be used to gain insights into microRNA precursor metabolism. , 2010, Journal of experimental botany.

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

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

[19]  Nam-Hai Chua,et al.  ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. , 2007, The Plant journal : for cell and molecular biology.

[20]  Thomas Girke,et al.  Cloning and Characterization of MicroRNAs from Ricew⃞ , 2005, The Plant Cell Online.

[21]  D. Weigel,et al.  Control of cell proliferation in Arabidopsis thaliana by microRNA miR396 , 2010, Development.

[22]  T. Jack.  Plant development going MADS , 2001, Plant Molecular Biology.

[23]  Noah Fahlgren,et al.  Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. , 2007, The Plant journal : for cell and molecular biology.

[24]  R. Russell,et al.  Animal MicroRNAs Confer Robustness to Gene Expression and Have a Significant Impact on 3′UTR Evolution , 2005, Cell.

[25]  Hong-Wei Xue,et al.  Control of Root Cap Formation by MicroRNA-Targeted Auxin Response Factors in Arabidopsisw⃞ , 2005, The Plant Cell Online.

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

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

[28]  Huanming Yang,et al.  Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. , 2010, Genome research.

[29]  Ivo L. Hofacker,et al.  Vienna RNA secondary structure server , 2003, Nucleic Acids Res..

[30]  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.

[31]  Hajime Sakai,et al.  Regulation of Flowering Time and Floral Organ Identity by a MicroRNA and Its APETALA2-Like Target Genes Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016238. , 2003, The Plant Cell Online.

[32]  Tobias Dezulian,et al.  Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. , 2007, Developmental cell.

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

[34]  Xiaofeng Cao,et al.  Degradome sequencing reveals endogenous small RNA targets in rice (Oryza sativa L. ssp. indica) , 2010, Frontiers in Biology.

[35]  Li Guo,et al.  The Fate of miRNA* Strand through Evolutionary Analysis: Implication for Degradation As Merely Carrier Strand or Potential Regulatory Molecule? , 2010, PloS one.

[36]  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..

[37]  Weixiong Zhang,et al.  Deep sequencing of small RNA libraries reveals dynamic regulation of conserved and novel microRNAs and microRNA-stars during silkworm development , 2010, BMC Genomics.

[38]  Jianhua Zhu,et al.  The Arabidopsis NFYA5 Transcription Factor Is Regulated Transcriptionally and Posttranscriptionally to Promote Drought Resistance[W] , 2008, The Plant Cell Online.

[39]  Sanghyuk Lee,et al.  MicroRNA genes are transcribed by RNA polymerase II , 2004, The EMBO journal.

[40]  Jonathan Pevsner,et al.  Basic Local Alignment Search Tool (BLAST) , 2005 .

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

[42]  J. Schwambach,et al.  Phenotypic Plasticity of Adventitious Rooting in Arabidopsis Is Controlled by Complex Regulation of AUXIN RESPONSE FACTOR Transcripts and MicroRNA Abundance[W] , 2009, The Plant Cell Online.

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

[44]  Detlef Weigel,et al.  The Sequential Action of miR156 and miR172 Regulates Developmental Timing in Arabidopsis , 2009, Cell.

[45]  Patrick Xuechun Zhao,et al.  psRNATarget: a plant small RNA target analysis server , 2011, Nucleic Acids Res..

[46]  M. Xie,et al.  Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes , 2005, Development.

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

[48]  H. Vaucheret,et al.  Plant ARGONAUTES. , 2008, Trends in plant science.

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

[50]  N. Rajewsky.  microRNA target predictions in animals , 2006, Nature Genetics.

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

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

[53]  Hai Huang,et al.  miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis , 2010, Journal of experimental botany.

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

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

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

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

[58]  Manolis Kellis,et al.  Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. , 2007, Genome research.

[59]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[60]  Zhen Su,et al.  EasyGO: Gene Ontology-based annotation and functional enrichment analysis tool for agronomical species , 2007, BMC Genomics.

[61]  N. Perrimon,et al.  Hierarchical rules for Argonaute loading in Drosophila. , 2009, Molecular cell.

[62]  C. Llave,et al.  Cleavage of Scarecrow-like mRNA Targets Directed by a Class of Arabidopsis miRNA , 2002, Science.