Arabidopsis lyrata Small RNAs: Transient MIRNA and Small Interfering RNA Loci within the Arabidopsis Genus[W][OA]

This study exploits the recent production of a draft nuclear genome sequence for Arabidopsis lyrata to examine evolution of plant MIRNA and p4-siRNA loci between two congenic Brassicaceae species. The results indicate that many MIRNAs and most p4-siRNA hot spots are rapidly changing and evolutionarily transient within the Arabidopsis genus. Twenty-one-nucleotide microRNAs (miRNAs) and 24-nucleotide Pol IV-dependent small interfering RNAs (p4-siRNAs) are the most abundant types of small RNAs in angiosperms. Some miRNAs are well conserved among different plant lineages, whereas others are less conserved, and it is not clear whether less-conserved miRNAs have the same functionality as the well conserved ones. p4-siRNAs are broadly produced in the Arabidopsis genome, sometimes from active hot spot loci, but it is unknown whether individual p4-siRNA hot spots are retained as hot spots between plant species. In this study, we compare small RNAs in two closely related species (Arabidopsis thaliana and Arabidopsis lyrata) and find that less-conserved miRNAs have high rates of divergence in MIRNA hairpin structures, mature miRNA sequences, and target-complementary sites in the other species. The fidelity of miRNA biogenesis from many less-conserved MIRNA hairpins frequently deteriorates in the sister species relative to the species of first discovery. We also observe that p4-siRNA occupied loci have a slight tendency to be retained as p4-siRNA loci between species, but the most active A. lyrata p4-siRNA hot spots are generally not syntenic to the most active p4-siRNA hot spots of A. thaliana. Altogether, our findings indicate that many MIRNAs and most p4-siRNA hot spots are rapidly changing and evolutionarily transient within the Arabidopsis genus.

[1]  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.

[2]  R. Doerge,et al.  Epigenetic Natural Variation in Arabidopsis thaliana , 2007, PLoS biology.

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

[4]  G. Ruvkun,et al.  A uniform system for microRNA annotation. , 2003, RNA.

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

[6]  M. Purugganan,et al.  Sequence Variation of MicroRNAs and Their Binding Sites in Arabidopsis1[W] , 2008, Plant Physiology.

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

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

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

[10]  A. Bucheton,et al.  Flamenco, a gene controlling the gypsy retrovirus of Drosophila melanogaster. , 1995, Genetics.

[11]  D. Bartel,et al.  Criteria for Annotation of Plant MicroRNAs , 2008, The Plant Cell Online.

[12]  D. Baulcombe,et al.  PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis , 2008, Proceedings of the National Academy of Sciences.

[13]  Doreen Ware,et al.  Evolution of Arabidopsis microRNA families through duplication events. , 2006, Genome research.

[14]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[15]  D. Huson,et al.  Evolution of Arabidopsis thaliana microRNAs from random sequences. , 2008, RNA.

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

[17]  C. Pikaard,et al.  RNA Polymerase V transcription guides ARGONAUTE4 to chromatin , 2009, Nature Genetics.

[18]  D. Haussler,et al.  Evolution's cauldron: Duplication, deletion, and rearrangement in the mouse and human genomes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. Bartel,et al.  Common Functions for Diverse Small RNAs of Land Plants[W][OA] , 2007, The Plant Cell Online.

[20]  Pamela J. Green,et al.  Role of RNA polymerase IV in plant small RNA metabolism , 2007, Proceedings of the National Academy of Sciences.

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

[22]  R. Lister,et al.  A link between RNA metabolism and silencing affecting Arabidopsis development. , 2008, Developmental cell.

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

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

[25]  Krystyna A. Kelly,et al.  Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis , 2009, Nature.

[26]  A. Mallory,et al.  MicroRNA-directed regulation: to cleave or not to cleave. , 2008, Trends in plant science.

[27]  M. Axtell.  Evolution of microRNAs and their targets: are all microRNAs biologically relevant? , 2008, Biochimica et biophysica acta.

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

[29]  Shivakundan Singh Tej,et al.  MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. , 2006, Genome research.

[30]  Manolis Kellis,et al.  Discrete Small RNA-Generating Loci as Master Regulators of Transposon Activity in Drosophila , 2007, Cell.

[31]  M. Axtell,et al.  Evolution of plant microRNAs and their targets. , 2008, Trends in plant science.

[32]  N. Lau,et al.  Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line. , 2009, Genome research.

[33]  S. Kauppinen,et al.  Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. , 2006, The Plant journal : for cell and molecular biology.

[34]  N. Warthmann,et al.  Comparative analysis of the MIR319a microRNA locus in Arabidopsis and related Brassicaceae. , 2008, Molecular biology and evolution.

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

[36]  Michael B. Stadler,et al.  MicroRNA-Mediated Regulation of Stomatal Development in Arabidopsis[W][OA] , 2007, The Plant Cell Online.

[37]  M. Matzke,et al.  RNA-mediated chromatin-based silencing in plants. , 2009, Current opinion in cell biology.

[38]  B. Liu,et al.  Small RNA-Directed Epigenetic Natural Variation in Arabidopsis thaliana , 2008, PLoS genetics.

[39]  Julius Brennecke,et al.  Specialized piRNA Pathways Act in Germline and Somatic Tissues of the Drosophila Ovary , 2009, Cell.

[40]  Michael Brudno,et al.  SHRiMP: Accurate Mapping of Short Color-space Reads , 2009, PLoS Comput. Biol..

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

[42]  D. Bartel,et al.  A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. , 2006, Genes & development.

[43]  Niels Gregersen,et al.  A Sequence variation , 1997 .

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

[45]  Ravi Sachidanandam,et al.  Developmentally Regulated piRNA Clusters Implicate MILI in Transposon Control , 2007, Science.

[46]  Shivakundan Singh Tej,et al.  Elucidation of the Small RNA Component of the Transcriptome , 2005, Science.

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