Finding MicroRNA Targets in Plants: Current Status and Perspectives

MicroRNAs (miRNAs), a class of ∼20–24 nt long non-coding RNAs, have critical roles in diverse biological processes including development, proliferation, stress response, etc. With the development and availability of experimental technologies and computational approaches, the field of miRNA biology has advanced tremendously over the last decade. By sequence complementarity, miRNAs have been estimated to regulate certain mRNA transcripts. Although it was once thought to be simple and straightforward to find plant miRNA targets, this viewpoint is being challenged by genetic and biochemical studies. In this review, we summarize recent progress in plant miRNA target recognition mechanisms, principles of target prediction, and introduce current experimental and computational tools for plant miRNA target prediction. At the end, we also present our thinking on the outlook for future directions in the development of plant miRNA target finding methods.

[1]  Scott A Givan,et al.  Genome-Wide Analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 Pathway in Arabidopsis Reveals Dependency on miRNA- and tasiRNA-Directed Targeting[W][OA] , 2007, The Plant Cell Online.

[2]  Rapid amplification of 5′ complementary DNA ends (5′ RACE) , 2005, Nature Methods.

[3]  Chi-Ying F. Huang,et al.  miRTarBase: a database curates experimentally validated microRNA–target interactions , 2010, Nucleic Acids Res..

[4]  Peter Drake,et al.  Data structures and algorithms in Java , 2005 .

[5]  Vikram Agarwal,et al.  Interspecies regulation of microRNAs and their targets. , 2008, Biochimica et biophysica acta.

[6]  Martin J. Simard,et al.  Argonaute proteins: key players in RNA silencing , 2008, Nature Reviews Molecular Cell Biology.

[7]  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.

[8]  H. D. Vanguilder,et al.  Twenty-five years of quantitative PCR for gene expression analysis. , 2008, BioTechniques.

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

[10]  Guiliang Tang,et al.  MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region , 2004 .

[11]  U. A. Ørom,et al.  MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. , 2008, Molecular cell.

[12]  Julie A. Law,et al.  Establishing, maintaining and modifying DNA methylation patterns in plants and animals , 2010, Nature Reviews Genetics.

[13]  V. Kim,et al.  Biogenesis of small RNAs in animals , 2009, Nature Reviews Molecular Cell Biology.

[14]  J. Mateos,et al.  A loop‐to‐base processing mechanism underlies the biogenesis of plant microRNAs miR319 and miR159 , 2009, The EMBO journal.

[15]  Tyler W. H. Backman,et al.  Update of ASRP: the Arabidopsis Small RNA Project database , 2007, Nucleic Acids Res..

[16]  B. Reinhart,et al.  The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans , 2000, Nature.

[17]  Jason S. Cumbie,et al.  High-Throughput Sequencing of Arabidopsis microRNAs: Evidence for Frequent Birth and Death of MIRNA Genes , 2007, PloS one.

[18]  E. Mardis Next-generation DNA sequencing methods. , 2008, Annual review of genomics and human genetics.

[19]  Ana Kozomara,et al.  miRBase: integrating microRNA annotation and deep-sequencing data , 2010, Nucleic Acids Res..

[20]  Janet Kelso,et al.  PatMaN: rapid alignment of short sequences to large databases , 2008, Bioinform..

[21]  Baohong Zhang,et al.  Bioinformatics Applications Note Data and Text Mining Target-align: a Tool for Plant Microrna Target Identification , 2022 .

[22]  Z. Yang,et al.  Computational identification of novel microRNAs and targets in Brassica napus , 2007, FEBS letters.

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

[24]  D. Bartel MicroRNAs: Target Recognition and Regulatory Functions , 2009, Cell.

[25]  H. Towbin,et al.  Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[26]  David P. Bartel,et al.  A Two-Hit Trigger for siRNA Biogenesis in Plants , 2006, Cell.

[27]  Costas S. Iliopoulos,et al.  An algorithm for mapping short reads to a dynamically changing genomic sequence , 2010, 2010 IEEE International Conference on Bioinformatics and Biomedicine (BIBM).

[28]  Shuigeng Zhou,et al.  imiRTP: An Integrated Method to Identifying miRNA-target Interactions in Arabidopsis thaliana , 2011, 2011 IEEE International Conference on Bioinformatics and Biomedicine.

[29]  Robert B Darnell,et al.  HITS‐CLIP: panoramic views of protein–RNA regulation in living cells , 2010, Wiley interdisciplinary reviews. RNA.

[30]  Mihaela Zavolan,et al.  Computational analysis of small RNA cloning data. , 2008, Methods.

[31]  M. Peter,et al.  Targeting of mRNAs by multiple miRNAs: the next step , 2010, Oncogene.

[32]  Weixiong Zhang,et al.  SeqTar: an effective method for identifying microRNA guided cleavage sites from degradome of polyadenylated transcripts in plants , 2011, Nucleic acids research.

[33]  Nina V. Fedoroff,et al.  RNA Secondary Structural Determinants of miRNA Precursor Processing in Arabidopsis , 2010, Current Biology.

[34]  Noah Fahlgren,et al.  Identification of MIR390a precursor processing-defective mutants in Arabidopsis by direct genome sequencing , 2009, Proceedings of the National Academy of Sciences.

[35]  D. Bartel,et al.  Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. , 2004, Molecular cell.

[36]  C. Bracken,et al.  Experimental strategies for microRNA target identification , 2011, Nucleic acids research.

[37]  Matthew B. Stocks,et al.  PAREsnip: a tool for rapid genome-wide discovery of small RNA/target interactions evidenced through degradome sequencing , 2012, Nucleic acids research.

[38]  Mark A McPeek,et al.  The phylogenetic distribution of metazoan microRNAs: insights into evolutionary complexity and constraint. , 2006, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[39]  Scott B. Dewell,et al.  Transcriptome-wide Identification of RNA-Binding Protein and MicroRNA Target Sites by PAR-CLIP , 2010, Cell.

[40]  L. Sieburth,et al.  Widespread Translational Inhibition by Plant miRNAs and siRNAs , 2008, Science.

[41]  Olivier Voinnet,et al.  Revisiting the principles of microRNA target recognition and mode of action , 2009, Nature Reviews Molecular Cell Biology.

[42]  Peter F. Stadler,et al.  ViennaRNA Package 2.0 , 2011, Algorithms for Molecular Biology.

[43]  Yves Van de Peer,et al.  Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences , 2004, Bioinform..

[44]  N. Roy,et al.  A comparison of analog and Next-Generation transcriptomic tools for mammalian studies. , 2011, Briefings in functional genomics.

[45]  Ji Hoon Ahn,et al.  AGO1-miR173 complex initiates phased siRNA formation in plants , 2008, Proceedings of the National Academy of Sciences.

[46]  Kenji Suzuki,et al.  A detailed investigation of accessibilities around target sites of siRNAs and miRNAs , 2011, Bioinform..

[47]  Tim R. Mercer,et al.  Global analysis of the mammalian RNA degradome reveals widespread miRNA-dependent and miRNA-independent endonucleolytic cleavage , 2011, Nucleic acids research.

[48]  G. Collins The next generation. , 2006, Scientific American.

[49]  John L. Bowman,et al.  Gene regulation: Ancient microRNA target sequences in plants , 2004, Nature.

[50]  P. Pandolfi,et al.  A ceRNA Hypothesis: The Rosetta Stone of a Hidden RNA Language? , 2011, Cell.

[51]  Robert D. Finn,et al.  Rfam: Wikipedia, clans and the “decimal” release , 2010, Nucleic Acids Res..

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

[53]  Sean R Eddy,et al.  How do RNA folding algorithms work? , 2004, Nature Biotechnology.

[54]  Yves Van de Peer,et al.  TAPIR, a web server for the prediction of plant microRNA targets, including target mimics , 2010, Bioinform..

[55]  Tanya Z. Berardini,et al.  The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools , 2011, Nucleic Acids Res..

[56]  Patrick Xuechun Zhao,et al.  Computational analysis of miRNA targets in plants: current status and challenges , 2011, Briefings Bioinform..

[57]  M. Schmid,et al.  Specific effects of microRNAs on the plant transcriptome. , 2005, Developmental cell.

[58]  Gang Wu,et al.  Nuclear processing and export of microRNAs in Arabidopsis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Tao Wang,et al.  PMRD: plant microRNA database , 2009, Nucleic Acids Res..

[60]  Uwe Ohler,et al.  High-resolution experimental and computational profiling of tissue-specific known and novel miRNAs in Arabidopsis. , 2012, Genome research.

[61]  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.

[62]  Francisco José Esteban,et al.  Next-generation bioinformatics: using many-core processor architecture to develop a web service for sequence alignment , 2010, Bioinform..

[63]  E. Lai,et al.  Vive la différence: biogenesis and evolution of microRNAs in plants and animals , 2011, Genome Biology.

[64]  Xuemei Chen,et al.  Methylation as a Crucial Step in Plant microRNA Biogenesis , 2005, Science.

[65]  Mihaela Zavolan,et al.  Relative contribution of sequence and structure features to the mRNA binding of Argonaute/EIF2C-miRNA complexes and the degradation of miRNA targets. , 2009, Genome research.

[66]  Detlef Weigel,et al.  Plant secondary siRNA production determined by microRNA-duplex structure , 2012, Proceedings of the National Academy of Sciences.

[67]  Duangdao Wichadakul,et al.  MicroPC (μPC): A comprehensive resource for predicting and comparing plant microRNAs , 2009, BMC Genomics.

[68]  Z. Chen,et al.  Roles of target site location and sequence complementarity in trans-acting siRNA formation in Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[69]  A. Pasquinelli MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship , 2012, Nature Reviews Genetics.

[70]  Ramanjulu Sunkar,et al.  Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome. , 2009, RNA.

[71]  P. Zamore,et al.  Small silencing RNAs: an expanding universe , 2009, Nature Reviews Genetics.

[72]  Josh T. Cuperus,et al.  Evolution and Functional Diversification of MIRNA Genes , 2011, Plant Cell.

[73]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

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

[75]  Xiao Li,et al.  Computational detection of microRNAs targeting transcription factor genes in Arabidopsis thaliana , 2005, Comput. Biol. Chem..

[76]  Tyson A. Clark,et al.  HITS-CLIP yields genome-wide insights into brain alternative RNA processing , 2008, Nature.

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

[78]  Y. Qi,et al.  Rice MicroRNA Effector Complexes and Targets[C][W] , 2009, The Plant Cell Online.

[79]  V. Ambros,et al.  The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 , 1993, Cell.

[80]  Christopher M. Player,et al.  Large-Scale Sequencing Reveals 21U-RNAs and Additional MicroRNAs and Endogenous siRNAs in C. elegans , 2006, Cell.

[81]  Vincent Moulton,et al.  A toolkit for analysing large-scale plant small RNA datasets , 2008, Bioinform..

[82]  S. Chi,et al.  An alternative mode of microRNA target recognition , 2012, Nature Structural &Molecular Biology.

[83]  E. Izaurralde,et al.  Gene silencing by microRNAs: contributions of translational repression and mRNA decay , 2011, Nature Reviews Genetics.

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

[85]  G. Nuovo,et al.  Experimental validation of miRNA targets. , 2008, Methods.

[86]  Dennis B. Troup,et al.  NCBI GEO: archive for functional genomics data sets—10 years on , 2010, Nucleic Acids Res..

[87]  Barbara Baker,et al.  SoMART: a web server for plant miRNA, tasiRNA and target gene analysis. , 2012, The Plant journal : for cell and molecular biology.

[88]  Albert Kim,et al.  Detecting miRNAs in deep-sequencing data: a software performance comparison and evaluation , 2013, Briefings Bioinform..

[89]  E. Lai Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation , 2002, Nature Genetics.

[90]  Xuemei Chen,et al.  Methylation Protects miRNAs and siRNAs from a 3′-End Uridylation Activity in Arabidopsis , 2005, Current Biology.

[91]  Cole Trapnell,et al.  Computational methods for transcriptome annotation and quantification using RNA-seq , 2011, Nature Methods.

[92]  R. Russell,et al.  Principles of MicroRNA–Target Recognition , 2005, PLoS biology.

[93]  Shuigeng Zhou,et al.  MiRenSVM: towards better prediction of microRNA precursors using an ensemble SVM classifier with multi-loop features , 2010, BMC Bioinformatics.

[94]  R. Overbeek,et al.  Searching for patterns in genomic data. , 1997, Trends in genetics : TIG.

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

[96]  L. Lim,et al.  MicroRNA targeting specificity in mammals: determinants beyond seed pairing. , 2007, Molecular cell.

[97]  Adam M. Gustafson,et al.  microRNA-Directed Phasing during Trans-Acting siRNA Biogenesis in Plants , 2005, Cell.

[98]  Webb Miller,et al.  CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets , 2009, Bioinform..

[99]  Dang D. Long,et al.  Potent effect of target structure on microRNA function , 2007, Nature Structural &Molecular Biology.

[100]  James C. Carrington,et al.  Specificity of ARGONAUTE7-miR390 Interaction and Dual Functionality in TAS3 Trans-Acting siRNA Formation , 2008, Cell.

[101]  Zhiping Weng,et al.  Target RNA–Directed Trimming and Tailing of Small Silencing RNAs , 2010, Science.

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

[103]  Shuigeng Zhou,et al.  miRFam: an effective automatic miRNA classification method based on n-grams and a multiclass SVM , 2011, BMC Bioinformatics.

[104]  B. Cullen,et al.  Viruses and microRNAs: RISCy interactions with serious consequences. , 2011, Genes & development.

[105]  J. Ule,et al.  iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution , 2010, Nature Structural &Molecular Biology.

[106]  V. Kim MicroRNA biogenesis: coordinated cropping and dicing , 2005, Nature Reviews Molecular Cell Biology.

[107]  Florian Buettner,et al.  The sufficient minimal set of miRNA seed types , 2011, Bioinform..

[108]  Yijun Qi,et al.  Biochemical specialization within Arabidopsis RNA silencing pathways. , 2005, Molecular cell.

[109]  David M. Goodstein,et al.  Phytozome: a comparative platform for green plant genomics , 2011, Nucleic Acids Res..

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

[111]  Shuigeng Zhou,et al.  Genome-wide search for miRNA-target interactions in Arabidopsis thaliana with an integrated approach , 2012, BMC Genomics.

[112]  Ashwani Jha,et al.  Employing machine learning for reliable miRNA target identification in plants , 2011, BMC Genomics.

[113]  John A. Hamilton,et al.  The TIGR Rice Genome Annotation Resource: improvements and new features , 2006, Nucleic Acids Res..

[114]  J. Steitz,et al.  Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5′ UTR as in the 3′ UTR , 2007, Proceedings of the National Academy of Sciences.

[115]  D. Bartel,et al.  The impact of microRNAs on protein output , 2008, Nature.

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

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

[118]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[119]  Gary Stacey,et al.  MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. , 2011, Genes & development.

[120]  Edwards Allen,et al.  miRNAs in the biogenesis of trans-acting siRNAs in higher plants. , 2010, Seminars in cell & developmental biology.

[121]  Nancy A Eckardt Investigating Translational Repression by MicroRNAs in Arabidopsis , 2009, The Plant Cell Online.

[122]  Detlef Weigel,et al.  Gene silencing in plants using artificial microRNAs and other small RNAs. , 2008, The Plant journal : for cell and molecular biology.

[123]  Ping Wu,et al.  PmiRKB: a plant microRNA knowledge base , 2010, Nucleic Acids Res..

[124]  G. Ruvkun,et al.  Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans , 1993, Cell.

[125]  B. Reinhart,et al.  Prediction of Plant MicroRNA Targets , 2002, Cell.

[126]  Hanah Margalit,et al.  RepTar: a database of predicted cellular targets of host and viral miRNAs , 2010, Nucleic Acids Res..

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

[128]  Kyle Kai-How Farh,et al.  Expanding the microRNA targeting code: functional sites with centered pairing. , 2010, Molecular cell.

[129]  Gregory J. Hannon,et al.  Diverse endonucleolytic cleavage sites in the mammalian transcriptome depend upon microRNAs, Drosha, and additional nucleases. , 2010, Molecular cell.

[130]  Rasko Leinonen,et al.  The sequence read archive: explosive growth of sequencing data , 2011, Nucleic Acids Res..

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

[132]  Weixiong Zhang,et al.  Multiple distinct small RNAs originate from the same microRNA precursors , 2010, Genome Biology.

[133]  Hui Zhou,et al.  starBase: a database for exploring microRNA–mRNA interaction maps from Argonaute CLIP-Seq and Degradome-Seq data , 2010, Nucleic Acids Res..

[134]  Detlef Weigel,et al.  Structure Determinants for Accurate Processing of miR172a in Arabidopsis thaliana , 2010, Current Biology.

[135]  D. Bartel MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[136]  Michael Kertesz,et al.  The role of site accessibility in microRNA target recognition , 2007, Nature Genetics.