Non-coding RNAs and Their Roles in Stress Response in Plants

Eukaryotic genomes encode thousands of non-coding RNAs (ncRNAs), which play crucial roles in transcriptional and post-transcriptional regulation of gene expression. Accumulating evidence indicates that ncRNAs, especially microRNAs (miRNAs) and long ncRNAs (lncRNAs), have emerged as key regulatory molecules in plant stress responses. In this review, we have summarized the current progress on the understanding of plant miRNA and lncRNA identification, characteristics, bioinformatics tools, and resources, and provided examples of mechanisms of miRNA- and lncRNA-mediated plant stress tolerance.

[1]  C. Zou,et al.  Combined small RNA and degradome sequencing reveals novel miRNAs and their targets in response to low nitrate availability in maize. , 2013, Annals of botany.

[2]  Min Chen,et al.  Genome-wide identification and characterization of novel lncRNAs in Populus under nitrogen deficiency , 2016, Molecular Genetics and Genomics.

[3]  Zhen Su,et al.  PNRD: a plant non-coding RNA database , 2014, Nucleic Acids Res..

[4]  Yun Xiao,et al.  MiRNA–miRNA synergistic network: construction via co-regulating functional modules and disease miRNA topological features , 2010, Nucleic acids research.

[5]  A. Harrison,et al.  The roles of cross-talk epigenetic patterns in Arabidopsis thaliana. , 2016, Briefings in functional genomics.

[6]  Zhao Zhang,et al.  MTide: an integrated tool for the identification of miRNA-target interaction in plants , 2015, Bioinform..

[7]  Hsien-Da Huang,et al.  RegRNA: an integrated web server for identifying regulatory RNA motifs and elements , 2006, Nucleic Acids Res..

[8]  Andreu Paytuví Gallart,et al.  GREENC: a Wiki-based database of plant lncRNAs , 2015, Nucleic Acids Res..

[9]  Yingyin Yao,et al.  Characterization of Small RNAs Derived from tRNAs, rRNAs and snoRNAs and Their Response to Heat Stress in Wheat Seedlings , 2016, PloS one.

[10]  Shihua Zhang,et al.  PLNlncRbase: A resource for experimentally identified lncRNAs in plants. , 2015, Gene.

[11]  Wei Wu,et al.  NONCODE 2016: an informative and valuable data source of long non-coding RNAs , 2015, Nucleic Acids Res..

[12]  Jing Xia,et al.  Endogenous small-noncoding RNAs and their roles in chilling response and stress acclimation in Cassava , 2014, BMC Genomics.

[13]  Olga Popova,et al.  The RdDM Pathway Is Required for Basal Heat Tolerance in Arabidopsis , 2013, Molecular plant.

[14]  Xiong-Hui Zhou,et al.  Functional analysis of long intergenic non-coding RNAs in phosphate-starved rice using competing endogenous RNA network , 2016, Scientific Reports.

[15]  Jiangbo Huang,et al.  Functional roles of histone modification, chromatin remodeling and microRNAs in Arabidopsis flower development. , 2013, International review of cell and molecular biology.

[16]  Duangdao Wichadakul,et al.  C-mii: a tool for plant miRNA and target identification , 2012, BMC Genomics.

[17]  Jian Zhang,et al.  PlantNATsDB: a comprehensive database of plant natural antisense transcripts , 2011, Nucleic Acids Res..

[18]  O. Borsani,et al.  Endogenous siRNAs Derived from a Pair of Natural cis-Antisense Transcripts Regulate Salt Tolerance in Arabidopsis , 2005, Cell.

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

[20]  Sudesh Kumar Yadav,et al.  Plant Small RNAs: Biogenesis, Mode of Action and Their Roles in Abiotic Stresses , 2011, Genom. Proteom. Bioinform..

[21]  Antonio J. Pérez-Pulido,et al.  Semirna: searching for plant miRNAs using target sequences. , 2012, Omics : a journal of integrative biology.

[22]  Lei Li,et al.  miRDeep-P: a computational tool for analyzing the microRNA transcriptome in plants , 2011, Bioinform..

[23]  J. Mattick,et al.  Small RNAs derived from snoRNAs. , 2009, RNA.

[24]  Abdoulaye Baniré Diallo,et al.  WMP: A novel comprehensive wheat miRNA database, including related bioinformatics software , 2015, bioRxiv.

[25]  Hikmet Budak,et al.  Stress responsive miRNAs and isomiRs in cereals. , 2015, Plant science : an international journal of experimental plant biology.

[26]  Andriy Bilichak,et al.  The elucidation of stress memory inheritance in Brassica rapa plants , 2015, Front. Plant Sci..

[27]  Marcel E. Dinger,et al.  lncRNAdb v2.0: expanding the reference database for functional long noncoding RNAs , 2014, Nucleic Acids Res..

[28]  J. Kocher,et al.  CPAT: Coding-Potential Assessment Tool using an alignment-free logistic regression model , 2013, Nucleic acids research.

[29]  S. Rhee,et al.  PlantMirnaT: miRNA and mRNA integrated analysis fully utilizing characteristics of plant sequencing data. , 2015, Methods.

[30]  Neeti Sanan-Mishra,et al.  Role of microRNAs in rice plant under salt stress , 2016 .

[31]  Jeff Schell,et al.  Soybean ENOD40 encodes two peptides that bind to sucrose synthase , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Cecilia Contreras-Cubas,et al.  Non-coding RNAs in the plant response to abiotic stress , 2012, Planta.

[33]  Huan Wang,et al.  Long noncoding RNA transcriptome of plants. , 2015, Plant biotechnology journal.

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

[35]  Ramanjulu Sunkar,et al.  Nutrient- and other stress-responsive microRNAs in plants: Role for thiol-based redox signaling , 2015, Plant signaling & behavior.

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

[37]  Ali Movahedi,et al.  RNA-directed DNA methylation in plants , 2015, Plant Cell Reports.

[38]  M. Todesco,et al.  Target mimicry provides a new mechanism for regulation of microRNA activity , 2007, Nature Genetics.

[39]  Yi Zhao,et al.  Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts , 2013, Nucleic acids research.

[40]  Meng Zhao,et al.  Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. , 2011, The New phytologist.

[41]  J. Riechmann,et al.  Small RNA profiling reveals regulation of Arabidopsis miR168 and heterochromatic siRNA415 in response to fungal elicitors , 2014, BMC Genomics.

[42]  Kenneth P. Nephew,et al.  BioVLAB-MMIA-NGS: microRNA-mRNA integrated analysis using high-throughput sequencing data , 2015, Bioinform..

[43]  Xue Liu,et al.  Long Non-coding RNAs and Their Biological Roles in Plants , 2015, Genom. Proteom. Bioinform..

[44]  R. Sunkar,et al.  Functions of microRNAs in plant stress responses. , 2012, Trends in plant science.

[45]  M. Szcześniak,et al.  CANTATAdb: A Collection of Plant Long Non-Coding RNAs , 2015, Plant & cell physiology.

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

[47]  Yongchao Dou,et al.  Regulation of miRNA abundance by RNA binding protein TOUGH in Arabidopsis , 2012, Proceedings of the National Academy of Sciences.

[48]  J. Guan,et al.  miRFANs: an integrated database for Arabidopsis thaliana microRNA function annotations , 2012, BMC Plant Biology.

[49]  Gang Liang,et al.  Identification of Nitrogen Starvation-Responsive MicroRNAs in Arabidopsis thaliana , 2012, PloS one.

[50]  M. Axtell Classification and comparison of small RNAs from plants. , 2013, Annual review of plant biology.

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

[52]  Jina,et al.  Mechanisms of small RNA generation from cis-NATs in response to environmental and developmental cues. , 2013, Molecular plant.

[53]  Weidong Yang,et al.  Erratum to “Biodistribution and SPECT Imaging Study of 99mTc Labeling NGR Peptide in Nude Mice Bearing Human HepG2 Hepatoma” , 2014, BioMed Research International.

[54]  J. A. Chekanova,et al.  Long non-coding RNAs and their functions in plants. , 2015, Current opinion in plant biology.

[55]  Bin Yu,et al.  CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts , 2013, Proceedings of the National Academy of Sciences.

[56]  M. S. Fedorova,et al.  The role of microRNA in abiotic stress response in plants , 2016, Molecular Biology.

[57]  Yajuan Wang,et al.  Long non-coding genes implicated in response to stripe rust pathogen stress in wheat (Triticum aestivum L.) , 2013, Molecular Biology Reports.

[58]  Li-Ching Hsieh,et al.  Abundance of tRNA-derived small RNAs in phosphate-starved Arabidopsis roots , 2010, Plant signaling & behavior.

[59]  Yadong Wang,et al.  TF2LncRNA: Identifying Common Transcription Factors for a List of lncRNA Genes from ChIP-Seq Data , 2014, BioMed research international.

[60]  Julia C. Engelmann,et al.  miRA: adaptable novel miRNA identification in plants using small RNA sequencing data , 2015, BMC Bioinformatics.

[61]  S. Machida,et al.  Crystal structure of Arabidopsis thaliana Dawdle forkhead-associated domain reveals a conserved phospho-threonine recognition cleft for dicer-like 1 binding. , 2013, Molecular plant.

[62]  Swati Megha,et al.  Genome Wide Identification and Functional Prediction of Long Non-Coding RNAs Responsive to Sclerotinia sclerotiorum Infection in Brassica napus , 2016, PloS one.

[63]  Caroline Dean,et al.  Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization , 2014, Proceedings of the National Academy of Sciences.

[64]  S. Asha,et al.  Transfer RNA Derived Small RNAs Targeting Defense Responsive Genes Are Induced during Phytophthora capsici Infection in Black Pepper (Piper nigrum L.) , 2016, Front. Plant Sci..

[65]  Masahiro Sugiura,et al.  A novel hypoxic stress-responsive long non-coding RNA transcribed by RNA polymerase III in Arabidopsis , 2012, RNA biology.

[66]  Stefano Lonardi,et al.  Mechanisms of small RNA generation from cis-NATs in response to environmental and developmental cues. , 2013, Molecular plant.

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

[68]  Qingli Guo,et al.  Identification of Maize Long Non-Coding RNAs Responsive to Drought Stress , 2014, PloS one.

[69]  Andrew P. Harrison,et al.  Genome-wide view of natural antisense transcripts in Arabidopsis thaliana , 2015, DNA research : an international journal for rapid publication of reports on genes and genomes.

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

[71]  Manolis Kellis,et al.  PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions , 2011, Bioinform..

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

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

[74]  Pritish Kumar Varadwaj,et al.  DeepLNC, a long non-coding RNA prediction tool using deep neural network , 2016, Network Modeling Analysis in Health Informatics and Bioinformatics.

[75]  A. Malhotra,et al.  A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). , 2009, Genes & development.

[76]  Bin Yu,et al.  PRL1, an RNA-Binding Protein, Positively Regulates the Accumulation of miRNAs and siRNAs in Arabidopsis , 2014, PLoS genetics.

[77]  Qianwen Sun,et al.  Functions of plants long non-coding RNAs. , 2016, Biochimica et biophysica acta.

[78]  V. Shriram,et al.  MicroRNAs As Potential Targets for Abiotic Stress Tolerance in Plants , 2016, Front. Plant Sci..

[79]  Zhengguo Li,et al.  SlAGO4A, a core factor of RNA-directed DNA methylation (RdDM) pathway, plays an important role under salt and drought stress in tomato , 2016, Molecular Breeding.

[80]  R. Amasino,et al.  FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering , 1999, Plant Cell.

[81]  Ana M. Aransay,et al.  miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments , 2009, Nucleic Acids Res..

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

[83]  Turgay Unver,et al.  miRNA-based drought regulation in wheat , 2015, Functional & Integrative Genomics.

[84]  Huan Wang,et al.  Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis , 2014, Genome research.

[85]  German Spangenberg,et al.  Role of microRNAs involved in plant response to nitrogen and phosphorous limiting conditions , 2015, Front. Plant Sci..

[86]  L. Stanton,et al.  Long noncoding RNAs in development and disease of the central nervous system. , 2013, Trends in genetics : TIG.

[87]  Douglas S. Domingues,et al.  PlanTE-MIR DB: a database for transposable element-related microRNAs in plant genomes , 2016, Functional & Integrative Genomics.

[88]  P. Manavella,et al.  miRNA Biogenesis: A Dynamic Pathway. , 2016, Trends in plant science.

[89]  Guodong Yang,et al.  Salt-induced transcription factor MYB74 is regulated by the RNA-directed DNA methylation pathway in Arabidopsis , 2015, Journal of experimental botany.

[90]  Xiaofeng Fang,et al.  Transcription and processing of primary microRNAs are coupled by Elongator complex in Arabidopsis , 2015, Nature Plants.

[91]  Anton J. Enright,et al.  spongeScan: A web for detecting microRNA binding elements in lncRNA sequences , 2016, Nucleic Acids Res..

[92]  B. Gregory,et al.  The Conservation and Function of RNA Secondary Structure in Plants. , 2016, Annual review of plant biology.

[93]  Weicong Qi,et al.  Genome-wide identification and functional prediction of nitrogen-responsive intergenic and intronic long non-coding RNAs in maize (Zea mays L.) , 2016, BMC Genomics.

[94]  Runsheng Chen,et al.  Genomic features and regulatory roles of intermediate-sized non-coding RNAs in Arabidopsis. , 2014, Molecular plant.

[95]  K. Sun,et al.  iSeeRNA: identification of long intergenic non-coding RNA transcripts from transcriptome sequencing data , 2013, BMC Genomics.

[96]  D. Rees,et al.  High-throughput sequencing reveals small RNAs involved in ASGV infection , 2014, BMC Genomics.

[97]  J. Rinn,et al.  Discovery and annotation of long noncoding RNAs , 2015, Nature Structural &Molecular Biology.

[98]  M. Keck,et al.  miRNAs and other non-coding RNAs in posttraumatic stress disorder: A systematic review of clinical and animal studies. , 2015, Journal of psychiatric research.

[99]  C. Pikaard,et al.  Noncoding Transcription by RNA Polymerase Pol IVb/Pol V Mediates Transcriptional Silencing of Overlapping and Adjacent Genes , 2008, Cell.

[100]  Jiang Shu,et al.  Dietary MicroRNA Database (DMD): An Archive Database and Analytic Tool for Food-Borne microRNAs , 2015, PloS one.

[101]  Mingming Xin,et al.  Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing , 2011, BMC Plant Biology.

[102]  Xuemei Chen,et al.  NOT2 Proteins Promote Polymerase II–Dependent Transcription and Interact with Multiple MicroRNA Biogenesis Factors in Arabidopsis[C][W] , 2013, Plant Cell.

[103]  Ruifeng Hu,et al.  lncRNATargets: A platform for lncRNA target prediction based on nucleic acid thermodynamics , 2016, J. Bioinform. Comput. Biol..

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

[105]  Detlef Weigel,et al.  Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity , 2016, eLife.

[106]  Yong Zhang,et al.  CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine , 2007, Nucleic Acids Res..

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

[108]  Renyi Liu,et al.  Genome-wide analysis of tomato long non-coding RNAs and identification as endogenous target mimic for microRNA in response to TYLCV infection , 2015, Scientific Reports.

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

[110]  Qian-Hao Zhu,et al.  DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis , 2014, Genome Biology.

[111]  Caroline Dean,et al.  Functional Consequences of Splicing of the Antisense Transcript COOLAIR on FLC Transcription , 2014, Molecular cell.

[112]  A. Werner,et al.  The functions of natural antisense transcripts. , 2013, Essays in biochemistry.

[113]  Sebastian D. Mackowiak,et al.  miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades , 2011, Nucleic acids research.

[114]  H. Sano,et al.  Expression of ZmMET1, a gene encoding a DNA methyltransferase from maize, is associated not only with DNA replication in actively proliferating cells, but also with altered DNA methylation status in cold-stressed quiescent cells. , 2000, Nucleic acids research.

[115]  Jiyuan An,et al.  miRPlant: an integrated tool for identification of plant miRNA from RNA sequencing data , 2014, BMC Bioinformatics.

[116]  Yan Guo,et al.  Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features. , 2014, The Plant journal : for cell and molecular biology.

[117]  Ana Kozomara,et al.  miRBase: annotating high confidence microRNAs using deep sequencing data , 2013, Nucleic Acids Res..

[118]  Robert D. Finn,et al.  Rfam 12.0: updates to the RNA families database , 2014, Nucleic Acids Res..

[119]  Ao Li,et al.  PASmiR: a literature-curated database for miRNA molecular regulation in plant response to abiotic stress , 2013, BMC Plant Biology.

[120]  Sibum Sung,et al.  Vernalization-Mediated Epigenetic Silencing by a Long Intronic Noncoding RNA , 2011, Science.

[121]  Julia A Chekanova,et al.  Arabidopsis RRP6L1 and RRP6L2 Function in FLOWERING LOCUS C Silencing via Regulation of Antisense RNA Synthesis , 2014, PLoS genetics.