Characterization of Small RNAs Derived from tRNAs, rRNAs and snoRNAs and Their Response to Heat Stress in Wheat Seedlings

Small RNAs (sRNAs) derived from non-coding RNAs (ncRNAs), such as tRNAs, rRNAs and snoRNAs, have been identified in various organisms. Several observations have indicated that cleavage of tRNAs and rRNAs is induced by various stresses. To clarify whether sRNAs in wheat derived from tRNAs (stRNAs), rRNAs (srRNAs) and snoRNAs (sdRNAs) are produced specifically in association with heat stress responses, we carried out a bioinformatic analysis of sRNA libraries from wheat seedlings and performed comparisons between control and high-temperature-treated samples to measure the differential abundance of stRNAs, srRNAs and sdRNAs. We found that the production of sRNAs from tRNAs, 5.8S rRNAs, and 28S rRNAs was more specific than that from 5S rRNAs and 18S rRNAs, and more than 95% of the stRNAs were processed asymmetrically from the 3’ or 5’ ends of mature tRNAs. We identified 333 stRNAs and 8,822 srRNAs that were responsive to heat stress. Moreover, the expression of stRNAs derived from tRNA-Val-CAC, tRNA-Thr-UGU, tRNA-Tyr-GUA and tRNA-Ser-UGA was not only up-regulated under heat stress but also induced by osmotic stress, suggesting that the increased cleavage of tRNAs might be a mechanism that developed in wheat seedlings to help them cope with adverse environmental conditions.

[1]  Zhanjie Li,et al.  Identification and characterization of microRNAs in the flag leaf and developing seed of wheat (Triticum aestivum L.) , 2014, BMC Genomics.

[2]  Yi Liu,et al.  qiRNA is a new type of small interfering RNA induced by DNA damage , 2009, Nature.

[3]  Masayuki Nashimoto,et al.  Modulation of Gene Expression by Human Cytosolic tRNase ZL through 5′-Half-tRNA , 2009, PloS one.

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

[5]  W. Karłowski,et al.  Transcriptionally and post-transcriptionally regulated microRNAs in heat stress response in barley , 2014, Journal of experimental botany.

[6]  Tao Pan,et al.  Angiogenin-Cleaved tRNA Halves Interact with Cytochrome c, Protecting Cells from Apoptosis during Osmotic Stress , 2014, Molecular and Cellular Biology.

[7]  S. S. Ajay,et al.  Identification and functional characterization of tRNA-derived RNA fragments (tRFs) in respiratory syncytial virus infection. , 2013, Molecular therapy : the journal of the American Society of Gene Therapy.

[8]  Daniel Gautheret,et al.  Genome-wide discovery and analysis of microRNAs and other small RNAs from rice embryogenic callus , 2011, RNA biology.

[9]  Markus Brameier,et al.  Human box C/D snoRNAs with miRNA like functions: expanding the range of regulatory RNAs , 2010, Nucleic Acids Res..

[10]  Yunliu Fan,et al.  Expression of zma-miR169 miRNAs and their target ZmNF-YA genes in response to abiotic stress in maize leaves. , 2015, Gene.

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

[12]  Yingyin Yao,et al.  Cloning and characterization of microRNAs from wheat (Triticum aestivum L.) , 2007, Genome Biology.

[13]  Hunseung Kang,et al.  Regulation of RNA metabolism in plant development and stress responses , 2013, Journal of Plant Biology.

[14]  V. Walbot,et al.  Spatiotemporally dynamic, cell-type–dependent premeiotic and meiotic phasiRNAs in maize anthers , 2015, Proceedings of the National Academy of Sciences.

[15]  G. Hutvagner,et al.  Small RNAs derived from the 5′ end of tRNA can inhibit protein translation in human cells , 2013, RNA biology.

[16]  K. Collins,et al.  Starvation-induced Cleavage of the tRNA Anticodon Loop in Tetrahymena thermophila* , 2005, Journal of Biological Chemistry.

[17]  J. Porter,et al.  Temperatures and the growth and development of wheat: a review , 1999 .

[18]  L. Marechal-Drouard,et al.  Surveillance and Cleavage of Eukaryotic tRNAs , 2015, International journal of molecular sciences.

[19]  Zhike Lu,et al.  Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice , 2014, Proceedings of the National Academy of Sciences.

[20]  Oliver H. Tam,et al.  Novel DICER-LIKE1 siRNAs Bypass the Requirement for DICER-LIKE4 in Maize Development[OPEN] , 2015, Plant Cell.

[21]  Lei Li,et al.  Identification and characterization of a subset of microRNAs in wheat (Triticum aestivum L.). , 2014, Genomics.

[22]  Weiwei Guo,et al.  Widespread, abundant, and diverse TE-associated siRNAs in developing wheat grain. , 2013, Gene.

[23]  Weiwei Guo,et al.  Whole-genome discovery of miRNAs and their targets in wheat (Triticum aestivum L.) , 2014, BMC Plant Biology.

[24]  N. Polacek,et al.  tRNA-Derived Fragments Target the Ribosome and Function as Regulatory Non-Coding RNA in Haloferax volcanii , 2012, Archaea.

[25]  R. Sunkar,et al.  Genome-Wide Discovery and Analysis of Phased Small Interfering RNAs in Chinese Sacred Lotus , 2014, PloS one.

[26]  Geoffrey J. Barton,et al.  Human miRNA Precursors with Box H/ACA snoRNA Features , 2009, PLoS Comput. Biol..

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

[28]  Yadan Luo,et al.  Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation , 2013, Nature.

[29]  E. Noor,et al.  Wheat Hybridization and Polyploidization Results in Deregulation of Small RNAs , 2011, Genetics.

[30]  Robert Blelloch,et al.  Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. , 2008, Genes & development.

[31]  Anita Marchfelder,et al.  High throughput sequencing reveals a plethora of small RNAs including tRNA derived fragments in Haloferax volcanii , 2012, RNA biology.

[32]  T. Pan,et al.  Genome-wide Identification and Quantitative Analysis of Cleaved tRNA Fragments Induced by Cellular Stress* , 2012, The Journal of Biological Chemistry.

[33]  Shoudong Zhang,et al.  The Phloem-Delivered RNA Pool Contains Small Noncoding RNAs and Interferes with Translation1[W][OA] , 2009, Plant Physiology.

[34]  Zhonghui Tang,et al.  Uncovering Small RNA-Mediated Responses to Cold Stress in a Wheat Thermosensitive Genic Male-Sterile Line by Deep Sequencing1[W][OA] , 2012, Plant Physiology.

[35]  Pavel Ivanov,et al.  Angiogenin-induced tRNA-derived Stress-induced RNAs Promote Stress-induced Stress Granule Assembly* , 2010, The Journal of Biological Chemistry.

[36]  Stefan Stamm,et al.  Processing of snoRNAs as a new source of regulatory non‐coding RNAs , 2013, BioEssays : news and reviews in molecular, cellular and developmental biology.

[37]  Michelle S. Scott,et al.  Human box C/D snoRNA processing conservation across multiple cell types , 2011, Nucleic acids research.

[38]  Yuan Chang,et al.  Extensive terminal and asymmetric processing of small RNAs from rRNAs, snoRNAs, snRNAs, and tRNAs , 2012, Nucleic acids research.

[39]  E. Mica,et al.  Post-transcriptional and post-translational regulations of drought and heat response in plants: a spider’s web of mechanisms , 2015, Front. Plant Sci..

[40]  Lu Wang,et al.  A novel class of heat-responsive small RNAs derived from the chloroplast genome of Chinese cabbage (Brassica rapa) , 2011, BMC Genomics.

[41]  David Tollervey,et al.  RNA in pieces. , 2011, Trends in genetics : TIG.

[42]  Michelle S. Scott,et al.  From snoRNA to miRNA: Dual function regulatory non-coding RNAs , 2011, Biochimie.

[43]  S. Yamasaki,et al.  Angiogenin cleaves tRNA and promotes stress-induced translational repression , 2009, The Journal of cell biology.

[44]  Steven P Gygi,et al.  Angiogenin-induced tRNA fragments inhibit translation initiation. , 2011, Molecular cell.

[45]  H. Liu,et al.  Development-associated microRNAs in grains of wheat (Triticum aestivumL.) , 2013, BMC Plant Biology.

[46]  H. Pathak,et al.  Novel and conserved heat-responsive microRNAs in wheat (Triticum aestivum L.) , 2014, Functional & Integrative Genomics.

[47]  Yun-Gui Yang,et al.  A Role for Small RNAs in DNA Double-Strand Break Repair , 2012, Cell.

[48]  Z. Yin,et al.  Identification and characterization of conserved microRNAs and their target genes in wheat (Triticum aestivum). , 2010, Genetics and molecular research : GMR.

[49]  S. Goldenberg,et al.  A population of tRNA-derived small RNAs is actively produced in Trypanosoma cruzi and recruited to specific cytoplasmic granules. , 2010, Molecular and biochemical parasitology.

[50]  Mingming Xin,et al.  Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.) , 2010, BMC Plant Biology.

[51]  Po-Jung Huang,et al.  A Comprehensive Expression Profile of MicroRNAs and Other Classes of Non-Coding Small RNAs in Barley Under Phosphorous-Deficient and -Sufficient Conditions , 2012, DNA research : an international journal for rapid publication of reports on genes and genomes.

[52]  H. Budak,et al.  miRNA expression patterns of Triticum dicoccoides in response to shock drought stress , 2011, Planta.

[53]  J. Lieberman,et al.  G-quadruplex structures contribute to the neuroprotective effects of angiogenin-induced tRNA fragments , 2014, Proceedings of the National Academy of Sciences.

[54]  T. Lion,et al.  Identification of RISC-Associated Adenoviral MicroRNAs, a Subset of Their Direct Targets, and Global Changes in the Targetome upon Lytic Adenovirus 5 Infection , 2014, Journal of Virology.

[55]  Xiaoyi Wei,et al.  Rice microRNA osa-miR1848 targets the obtusifoliol 14α-demethylase gene OsCYP51G3 and mediates the biosynthesis of phytosterols and brassinosteroids during development and in response to stress. , 2015, The New phytologist.

[56]  G. Yin,et al.  Combined Small RNA and Degradome Sequencing Reveals Novel MiRNAs and Their Targets in the High-Yield Mutant Wheat Strain Yunong 3114 , 2015, PloS one.

[57]  Wen-Hsiung Li,et al.  Uncovering Small RNA-Mediated Responses to Phosphate Deficiency in Arabidopsis by Deep Sequencing1[W][OA] , 2009, Plant Physiology.

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

[59]  Franck Vazquez,et al.  Arabidopsis endogenous small RNAs: highways and byways. , 2006, Trends in plant science.

[60]  Rogerio Margis,et al.  Description of plant tRNA-derived RNA fragments (tRFs) associated with argonaute and identification of their putative targets , 2013, Biology Direct.

[61]  G. Barton,et al.  Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. , 2009, RNA.

[62]  N. Rajewsky,et al.  A human snoRNA with microRNA-like functions. , 2008, Molecular cell.

[63]  A. Datta,et al.  Small RNAs in plants: recent development and application for crop improvement , 2015, Front. Plant Sci..

[64]  Andrea Califano,et al.  tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma , 2013, Proceedings of the National Academy of Sciences.

[65]  Marta Matvienko,et al.  Small RNAs, DNA methylation and transposable elements in wheat , 2010, BMC Genomics.

[66]  Haiyan Wu,et al.  Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array , 2008, BMC Genomics.

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

[68]  Mihaela Zavolan,et al.  The snoRNA MBII-52 (SNORD 115) is processed into smaller RNAs and regulates alternative splicing. , 2010, Human molecular genetics.

[69]  Harry F. Noller,et al.  Crystal Structure of a 70S Ribosome-tRNA Complex Reveals Functional Interactions and Rearrangements , 2014, Cell.

[70]  J. Rogers,et al.  Slicing the wheat genome , 2014, Science.

[71]  D. Haussecker,et al.  Human tRNA-derived small RNAs in the global regulation of RNA silencing. , 2010, RNA.

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

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

[74]  J. Batley,et al.  A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome , 2014, Science.

[75]  Ashesh A. Saraiya,et al.  snoRNA, a Novel Precursor of microRNA in Giardia lamblia , 2008, PLoS pathogens.

[76]  C. Bracken,et al.  Assessing the gene regulatory properties of Argonaute-bound small RNAs of diverse genomic origin , 2014, Nucleic acids research.

[77]  G. Hu,et al.  Emerging role of angiogenin in stress response and cell survival under adverse conditions , 2012, Journal of cellular physiology.

[78]  Fang Zhang,et al.  Profiling and Identification of Small rDNA-Derived RNAs and Their Potential Biological Functions , 2013, PloS one.

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

[80]  Yun Zheng,et al.  Characterization of small RNAs and their target genes in wheat seedlings using sequencing-based approaches. , 2013, Plant science : an international journal of experimental plant biology.