Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana

MicroRNAs (miRNAs) in plants and animals function as post-transcriptional regulators of target genes, many of which are involved in multicellular development. miRNAs guide effector complexes to target mRNAs through base-pair complementarity, facilitating site-specific cleavage or translational repression. Biogenesis of miRNAs involves nucleolytic processing of a precursor transcript with extensive foldback structure. Here, we provide evidence that genes encoding miRNAs in plants originated by inverted duplication of target gene sequences. Several recently evolved genes encoding miRNAs in Arabidopsis thaliana and other small RNA–generating loci possess the hallmarks of inverted duplication events that formed the arms on each side of their respective foldback precursors. We propose a model for miRNA evolution that suggests a mechanism for de novo generation of new miRNA genes with unique target specificities.

[1]  J. Bowman,et al.  Radial Patterning of Arabidopsis Shoots by Class III HD-ZIP and KANADI Genes , 2003, Current Biology.

[2]  Marjori Matzke,et al.  Evidence for Nuclear Processing of Plant Micro RNA and Short Interfering RNA Precursors1[w] , 2003, Plant Physiology.

[3]  M. A. Rector,et al.  Endogenous and Silencing-Associated Small RNAs in Plants Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.003210. , 2002, The Plant Cell Online.

[4]  Sean R. Eddy,et al.  Rfam: an RNA family database , 2003, Nucleic Acids Res..

[5]  Edwards Allen,et al.  P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction. , 2003, Developmental cell.

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

[7]  S. Teichmann,et al.  Gene regulatory network growth by duplication , 2004, Nature Genetics.

[8]  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.

[9]  Alan Herbert,et al.  The four Rs of RNA-directed evolution , 2003, Nature Genetics.

[10]  Neff Walker,et al.  A MicroRNA as a Translational Repressor of APETALA2 in Arabidopsis Flower Development , 2004 .

[11]  Patrick Achard,et al.  Modulation of floral development by a gibberellin-regulated microRNA , 2004, Development.

[12]  Elliot M Meyerowitz,et al.  Plants Compared to Animals: The Broadest Comparative Study of Development , 2002, Science.

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

[14]  D. Higgins,et al.  T-Coffee: A novel method for fast and accurate multiple sequence alignment. , 2000, Journal of molecular biology.

[15]  D. Bartel,et al.  Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs , 2004, Nature Reviews Genetics.

[16]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

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

[18]  B. Reinhart,et al.  Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA , 2000, Nature.

[19]  J. Messing,et al.  CARPEL FACTORY, a Dicer Homolog, and HEN1, a Novel Protein, Act in microRNA Metabolism in Arabidopsis thaliana , 2002, Current Biology.

[20]  Animesh Ray,et al.  DICER-LIKE1: blind men and elephants in Arabidopsis development. , 2002, Trends in plant science.

[21]  Franck Vazquez,et al.  Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. , 2004, Molecular cell.

[22]  A. Pasquinelli,et al.  A Cellular Function for the RNA-Interference Enzyme Dicer in the Maturation of the let-7 Small Temporal RNA , 2001, Science.

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

[24]  H. Vaucheret,et al.  The Nuclear dsRNA Binding Protein HYL1 Is Required for MicroRNA Accumulation and Plant Development, but Not Posttranscriptional Transgene Silencing , 2004, Current Biology.

[25]  David P. Bartel,et al.  MicroRNAs: At the Root of Plant Development?1 , 2003, Plant Physiology.

[26]  Yuichiro Watanabe,et al.  Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[28]  G. Hannon,et al.  C . elegans involved in developmental timing in Dicer functions in RNA interference and in synthesis of small RNA , 2001 .

[29]  Nature Genetics , 1991, Nature.

[30]  Adam M. Gustafson,et al.  Genetic and Functional Diversification of Small RNA Pathways in Plants , 2004, PLoS biology.

[31]  Z. Xie,et al.  Negative Feedback Regulation of Dicer-Like1 in Arabidopsis by microRNA-Guided mRNA Degradation , 2003, Current Biology.

[32]  M. Holder,et al.  Phylogeny estimation: traditional and Bayesian approaches , 2003, Nature Reviews Genetics.

[33]  E. Finnegan,et al.  The small RNA world , 2003, Journal of Cell Science.

[34]  Franck Vazquez,et al.  The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. , 2004, Genes & development.

[35]  B. Reinhart,et al.  MicroRNAs in plants. , 2002, Genes & development.

[36]  Poethig Rs,et al.  Life with 25,000 genes. , 2001 .

[37]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[38]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[39]  Diana V. Dugas,et al.  MicroRNA Regulation of NAC-Domain Targets Is Required for Proper Formation and Separation of Adjacent Embryonic, Vegetative, and Floral Organs , 2004, Current Biology.

[40]  Matthew Hurles,et al.  Gene Duplication: The Genomic Trade in Spare Parts , 2004, PLoS biology.

[41]  R S Poethig.  Life with 25,000 genes. , 2001, Genome research.

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

[43]  Olivier Voinnet,et al.  RETRACTED: Probing the MicroRNA and Small Interfering RNA Pathways with Virus-Encoded Suppressors of RNA Silencing[W] , 2004, Plant Cell.

[44]  Javier F. Palatnik,et al.  Control of leaf morphogenesis by microRNAs , 2003, Nature.

[45]  Gang Wu,et al.  SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. , 2004, Genes & development.

[46]  V. Kim,et al.  The nuclear RNase III Drosha initiates microRNA processing , 2003, Nature.

[47]  R. Tjian,et al.  Transcription regulation and animal diversity , 2003, Nature.

[48]  R. Sunkar,et al.  Novel and Stress-Regulated MicroRNAs and Other Small RNAs from Arabidopsis , 2004, The Plant Cell Online.

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

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

[51]  Patrick Laufs,et al.  MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems , 2004, Development.

[52]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..