Long non-coding RNAs

The biological relevance of long non-coding RNAs (lncRNAs) is emerging. Whether the lncRNAs could form structured precursors for small RNAs (sRNAs) production remains elusive. Here, 172 713 DCL1 (Dicer-like 1)-dependent sRNAs were identified in Arabidopsis. Except for the sRNAs mapped onto the microRNA precursors, the remaining ones led us to investigate their originations. Intriguingly, 65 006 sRNAs found their loci on 5891 lncRNAs. These sRNAs were sent to AGO (Argonaute) enrichment analysis. As a result, 1264 sRNAs were enriched in AGO1, which were then subjected to target prediction. Based on degradome sequencing data, 109 transcripts were validated to be targeted by 96 sRNAs. Besides, 44 lncRNAs were targeted by 23 sRNAs. To further support the origination of the DCL1-dependent sRNAs from lncRNAs, we searched for the degradome-based cleavage signals at either ends of the sRNA loci, which were supposed to be produced during DCL1-mediated processing of the long-stem structures. As a result, 63 612 loci were supported by degradome signatures. Among these loci, 6606 reside within the dsRNA-seq (double-stranded RNA sequencing) read-covered regions of 100 nt or longer. These regions were subjected to secondary structure prediction. And, 43 regions were identified to be capable of forming highly complementary long-stem structures. We proposed that these local long-stem structures could be recognized by DCL1 for cropping, thus serving as the sRNA precursors. We hope that our study could inspire more research efforts to study on the biological roles of the lncRNAs in plants.

[1]  V. Chiang,et al.  Adenylation of plant miRNAs , 2009, Nucleic acids research.

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

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

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

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

[6]  Caroline Dean,et al.  Long non-coding RNAs and chromatin regulation. , 2011, Current opinion in plant biology.

[7]  M. Van Montagu,et al.  Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. , 1994, The Plant cell.

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

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

[10]  T. Derrien,et al.  The Long Non-Coding RNAs: A New (P)layer in the “Dark Matter” , 2012, Front. Gene..

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

[12]  Ciro Indolfi,et al.  Non-Coding RNAs: The “Dark Matter” of Cardiovascular Pathophysiology , 2013, International journal of molecular sciences.

[13]  Meng Wang,et al.  Widespread Long Noncoding RNAs as Endogenous Target Mimics for MicroRNAs in Plants1[W] , 2013, Plant Physiology.

[14]  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.

[15]  S. Wyman,et al.  Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. , 2011, Genome research.

[16]  D. Bartel,et al.  MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. , 2010, Genes & development.

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

[18]  Photo and hormonal control of meristem identity in the Arabidopsis flower mutants apetala2 and apetala1. , 1997, The Plant cell.

[19]  P. Ryvkin,et al.  Genome-Wide Double-Stranded RNA Sequencing Reveals the Functional Significance of Base-Paired RNAs in Arabidopsis , 2010, PLoS genetics.

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

[21]  J L Bowman,et al.  Genes directing flower development in Arabidopsis. , 1989, The Plant cell.

[22]  Zhou Du,et al.  PlantGSEA: a gene set enrichment analysis toolkit for plant community , 2013, Nucleic Acids Res..

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

[24]  N. Chua,et al.  Genome-Wide Analysis Uncovers Regulation of Long Intergenic Noncoding RNAs in Arabidopsis[C][W] , 2012, Plant Cell.

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

[26]  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.

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

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

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

[30]  David Penny,et al.  The RNA infrastructure: dark matter of the eukaryotic cell? , 2009, Trends in genetics : TIG.

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

[32]  Edwards Allen,et al.  DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[34]  Ming Chen,et al.  A reversed framework for the identification of microRNA-target pairs in plants , 2013, Briefings Bioinform..

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

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

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

[38]  A. Wierzbicki.  The role of long non-coding RNA in transcriptional gene silencing. , 2012, Current opinion in plant biology.

[39]  S. Cohen,et al.  microRNA functions. , 2007, Annual review of cell and developmental biology.

[40]  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..

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

[42]  Huan Wang,et al.  PLncDB: plant long non-coding RNA database , 2013, Bioinform..