Small RNAs as big players in plant abiotic stress responses and nutrient deprivation.

Abiotic stress is one of the primary causes of crop losses worldwide. Much progress has been made in unraveling the complex stress response mechanisms, particularly in the identification of stress responsive protein-coding genes. In addition to protein coding genes, recently discovered microRNAs (miRNAs) and endogenous small interfering RNAs (siRNAs) have emerged as important players in plant stress responses. Initial clues suggesting that small RNAs are involved in plant stress responses stem from studies showing stress regulation of miRNAs and endogenous siRNAs, as well as from target predictions for some miRNAs. Subsequent studies have demonstrated an important functional role for these small RNAs in abiotic stress responses. This review focuses on recent advances, with emphasis on integration of small RNAs in stress regulatory networks.

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

[2]  D. Kliebenstein,et al.  Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. , 1998, Plant physiology.

[3]  Hailing Jin,et al.  A pathogen-inducible endogenous siRNA in plant immunity , 2006, Proceedings of the National Academy of Sciences.

[4]  Chun-Lin Su,et al.  Regulation of Phosphate Homeostasis by MicroRNA in Arabidopsis[W] , 2005, The Plant Cell Online.

[5]  L. Björn,et al.  Arabidopsis RADICAL-INDUCED CELL DEATH1 is involved in UV-B signaling , 2009, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[6]  H. Vaucheret,et al.  Functions of microRNAs and related small RNAs in plants , 2006, Nature Genetics.

[7]  N. Chua,et al.  MicroRNA Directs mRNA Cleavage of the Transcription Factor NAC1 to Downregulate Auxin Signals for Arabidopsis Lateral Root Development , 2005, The Plant Cell Online.

[8]  Rithy K. Roth,et al.  Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays , 2000, Nature Biotechnology.

[9]  S. Fukai,et al.  EFFECTS OF SOIL WATER DEFICIT AT DIFFERENT GROWTH STAGES ON RICE GROWTH AND YIELD UNDER UPLAND CONDITIONS. 1. GROWTH DURING DROUGHT , 1996 .

[10]  R. Sunkar,et al.  Drought and Salt Tolerance in Plants , 2005 .

[11]  M. Van Montagu,et al.  Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[12]  R. Sunkar,et al.  Posttranscriptional Induction of Two Cu/Zn Superoxide Dismutase Genes in Arabidopsis Is Mediated by Downregulation of miR398 and Important for Oxidative Stress Tolerance[W] , 2006, The Plant Cell Online.

[13]  C. Ticconi,et al.  Phosphate sensing in higher plants. , 2002, Physiologia plantarum.

[14]  L. Mao,et al.  Molecular evolution of the rice miR395 gene family , 2005, Cell Research.

[15]  H. Yokoyama,et al.  Geographical variation in heading characters among wheat landraces, Triticum aestivum L., and its implication for their adaptability , 1992, Theoretical and Applied Genetics.

[16]  Jian-Kang Zhu,et al.  A miRNA Involved in Phosphate-Starvation Response in Arabidopsis , 2005, Current Biology.

[17]  D. Baulcombe RNA silencing in plants , 2004, Nature.

[18]  N. Fedoroff,et al.  A Mutation in the Arabidopsis HYL1 Gene Encoding a dsRNA Binding Protein Affects Responses to Abscisic Acid, Auxin, and Cytokinin , 2000, Plant Cell.

[19]  Diana V. Dugas,et al.  MicroRNA regulation of gene expression in plants. , 2004, Current opinion in plant biology.

[20]  Vincent L. Chiang,et al.  Novel and Mechanical Stress–Responsive MicroRNAs in Populus trichocarpa That Are Absent from Arabidopsisw⃞ , 2005, The Plant Cell Online.

[21]  J. Bowman,et al.  Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots , 2001, Nature.

[22]  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.

[23]  M. J. Harrison,et al.  Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. , 2006, The Plant journal : for cell and molecular biology.

[24]  F. Gubler,et al.  The Arabidopsis GAMYB-Like Genes, MYB33 and MYB65, Are MicroRNA-Regulated Genes That Redundantly Facilitate Anther Development , 2005, The Plant Cell Online.

[25]  K. Shinozaki,et al.  Gene networks involved in drought stress response and tolerance. , 2006, Journal of experimental botany.

[26]  V. Ambros,et al.  The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 , 1993, Cell.

[27]  H. Hirt,et al.  Reactive oxygen species: metabolism, oxidative stress, and signal transduction. , 2004, Annual review of plant biology.

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

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

[30]  H. Marschner Mineral Nutrition of Higher Plants , 1988 .

[31]  D. Inzé,et al.  Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. , 1991, The EMBO journal.

[32]  Hai Huang,et al.  SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

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

[34]  Scott A. Givan,et al.  ASRP: the Arabidopsis Small RNA Project Database , 2004, Nucleic Acids Res..

[35]  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.

[36]  C. Kidner,et al.  The developmental role of microRNA in plants. , 2005, Current opinion in plant biology.

[37]  M. Xie,et al.  Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes , 2005, Development.

[38]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[39]  K. Akiyama,et al.  Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. , 2002, The Plant journal : for cell and molecular biology.

[40]  G. Dreyfuss,et al.  Messenger-RNA-binding proteins and the messages they carry , 2002, Nature Reviews Molecular Cell Biology.

[41]  B. Touraine,et al.  Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. , 1999, The Plant journal : for cell and molecular biology.

[42]  V. Ambros,et al.  Role of MicroRNAs in Plant and Animal Development , 2003, Science.

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

[44]  S. Kempa,et al.  Effect of sulfur availability on the integrity of amino acid biosynthesis in plants , 2006, Amino Acids.

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

[46]  Thomas Girke,et al.  Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[47]  J. Bailey-Serres,et al.  Regulation of translational initiation in plants. , 2002, Current opinion in plant biology.

[48]  F. W. Smith,et al.  The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. , 2000, The Plant journal : for cell and molecular biology.

[49]  Yiyue Zhang,et al.  The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[50]  E. Delhaize,et al.  Characterization of a Phosphate-Accumulator Mutant of Arabidopsis thaliana , 1995, Plant Physiology.

[51]  Joseph M. Dale,et al.  Empirical Analysis of Transcriptional Activity in the Arabidopsis Genome , 2003, Science.

[52]  Huan Wang,et al.  Prediction of trans-antisense transcripts in Arabidopsis thaliana , 2006, Genome Biology.

[53]  G. Ruvkun,et al.  Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans , 1993, Cell.

[54]  R. Jansen,et al.  mRNA localization and the cytoskeleton. , 2004, Current opinion in cell biology.

[55]  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.

[56]  V. Ambros The functions of animal microRNAs , 2004, Nature.

[57]  E. Baena-González,et al.  Sugar sensing and signaling in plants: conserved and novel mechanisms. , 2006, Annual review of plant biology.

[58]  R. Poethig,et al.  A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. , 2005, Genes & development.

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

[60]  Javier F. Palatnik,et al.  Specific effects of microRNAs on the plant transcriptome. , 2005, Developmental cell.

[61]  J. Bailey-Serres,et al.  Water-deficit-induced translational control in Nicotiana tabacum , 2003 .

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

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

[64]  Jonathan D. G. Jones,et al.  A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling , 2006, Science.

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

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

[67]  D. Bartel,et al.  MicroRNA-Directed Regulation of Arabidopsis AUXIN RESPONSE FACTOR17 Is Essential for Proper Development and Modulates Expression of Early Auxin Response Genesw⃞ , 2005, The Plant Cell Online.

[68]  G. Soldà,et al.  Shedding Light on the Dark Side of the Genome: Overlapping Genes in Higher Eukaryotes , 2004 .

[69]  D. Zilberman,et al.  RNA Silencing Genes Control de Novo DNA Methylation , 2004, Science.

[70]  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.

[71]  R. Mittler,et al.  Reactive oxygen gene network of plants. , 2004, Trends in plant science.

[72]  Terry Gaasterland,et al.  Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana , 2005, Genome Biology.

[73]  Cathie Martin,et al.  SERRATE: a new player on the plant microRNA scene , 2006, EMBO reports.

[74]  K. Raghothama Molecular Regulation of Phosphate Acquisition in Plants , 1999 .

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

[76]  Jianhua Zhu,et al.  Gene regulation during cold acclimation in plants , 2006 .

[77]  R. Martienssen,et al.  MicroRNA-Targeted and Small Interfering RNA–Mediated mRNA Degradation Is Regulated by Argonaute, Dicer, and RNA-Dependent RNA Polymerase in Arabidopsis[W][OA] , 2006, The Plant Cell Online.

[78]  M. Stitt,et al.  PHO2, MicroRNA399, and PHR1 Define a Phosphate-Signaling Pathway in Plants1[W][OA] , 2006, Plant Physiology.

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

[80]  Thomas Girke,et al.  Cloning and Characterization of MicroRNAs from Ricew⃞ , 2005, The Plant Cell Online.

[81]  D. Hoisington,et al.  Identification of quantitative trait loci under drought conditions in tropical maize. 1. Flowering parameters and the anthesis-silking interval , 1996, Theoretical and Applied Genetics.

[82]  M. Thomashow,et al.  Arabidopsis Transcriptome Profiling Indicates That Multiple Regulatory Pathways Are Activated during Cold Acclimation in Addition to the CBF Cold Response Pathway Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1 , 2002, The Plant Cell Online.

[83]  D. Inzé,et al.  Arabidopsis RADICAL-INDUCED CELL DEATH1 Belongs to the WWE Protein–Protein Interaction Domain Protein Family and Modulates Abscisic Acid, Ethylene, and Methyl Jasmonate Responses , 2004, The Plant Cell Online.

[84]  P. Zimmermann,et al.  GENEVESTIGATOR. Arabidopsis Microarray Database and Analysis Toolbox1[w] , 2004, Plant Physiology.

[85]  Chun-Lin Su,et al.  pho2, a Phosphate Overaccumulator, Is Caused by a Nonsense Mutation in a MicroRNA399 Target Gene1[W] , 2006, Plant Physiology.

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

[87]  Y. Poirier,et al.  Phosphate Transport and Homeostasis in Arabidopsis , 2002, The arabidopsis book.

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

[89]  Jian-Kang Zhu,et al.  ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. , 2003, Genes & development.

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

[91]  M. Hentze,et al.  Molecular mechanisms of translational control , 2004, Nature Reviews Molecular Cell Biology.

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