Comprehensive transcriptome analysis of auxin responses in Arabidopsis.

In plants, the hormone auxin shapes gene expression to regulate growth and development. Despite the detailed characterization of auxin-inducible genes, a comprehensive overview of the temporal and spatial dynamics of auxin-regulated gene expression is lacking. Here, we analyze transcriptome data from many publicly available Arabidopsis profiling experiments and assess tissue-specific gene expression both in response to auxin concentration and exposure time and in relation to other plant growth regulators. Our analysis shows that the primary response to auxin over a wide range of auxin application conditions and in specific tissues comprises almost exclusively the up-regulation of genes and identifies the most robust auxin marker genes. Tissue-specific auxin responses correlate with differential expression of Aux/IAA genes and the subsequent regulation of context- and sequence-specific patterns of gene expression. Changes in transcript levels were consistent with a distinct sequence of conjugation, increased transport capacity and down-regulation of biosynthesis in the temperance of high cellular auxin concentrations. Our data show that auxin regulates genes associated with the biosynthesis, catabolism and signaling pathways of other phytohormones. We present a transcriptional overview of the auxin response. Specific interactions between auxin and other phytohormones are highlighted, particularly the regulation of their metabolism. Our analysis provides a roadmap for auxin-dependent processes that underpins the concept of an 'auxin code'--a tissue-specific fingerprint of gene expression that initiates specific developmental processes.

[1]  S. Schreiber,et al.  SIR1, an Upstream Component in Auxin Signaling Identified by Chemical Genetics , 2003, Science.

[2]  Yukihisa Shimada,et al.  Brassinolide Induces IAA5, IAA19, and DR5, a Synthetic Auxin Response Element in Arabidopsis, Implying a Cross Talk Point of Brassinosteroid and Auxin Signaling , 2003, Plant Physiology.

[3]  P. Hurban,et al.  The auxin-induced transcriptome for etiolated Arabidopsis seedlings using a structure/function approach , 2003, Functional & Integrative Genomics.

[4]  M. Menges,et al.  The D-Type Cyclin CYCD3;1 Is Limiting for the G1-to-S-Phase Transition in Arabidopsis[W] , 2006, The Plant Cell Online.

[5]  M. Menges,et al.  Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. , 2002, The Plant journal : for cell and molecular biology.

[6]  G. Hagen,et al.  AUX/IAA Proteins Are Active Repressors, and Their Stability and Activity Are Modulated by Auxin Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010289. , 2001, The Plant Cell Online.

[7]  D. Inzé,et al.  Transcriptomic Footprints Disclose Specificity of Reactive Oxygen Species Signaling in Arabidopsis1[W] , 2006, Plant Physiology.

[8]  Walter P. Suza,et al.  Characterization of an Arabidopsis Enzyme Family That Conjugates Amino Acids to Indole-3-Acetic Acidw⃞ , 2005, The Plant Cell Online.

[9]  M. Caboche,et al.  Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. , 1998, The Plant journal : for cell and molecular biology.

[10]  J R Ecker,et al.  EIN4 and ERS2 Are Members of the Putative Ethylene Receptor Gene Family in Arabidopsis , 1998, Plant Cell.

[11]  J. Ecker,et al.  Ethylene signaling: from mutants to molecules. , 2000, Current opinion in plant biology.

[12]  T. Mockler,et al.  Interdependency of Brassinosteroid and Auxin Signaling in Arabidopsis , 2004, PLoS biology.

[13]  Zhenbiao Yang,et al.  Brassinosteroids Interact with Auxin to Promote Lateral Root Development in Arabidopsis1 , 2004, Plant Physiology.

[14]  D. Alabadí,et al.  Transcriptional Regulation of Gibberellin Metabolism Genes by Auxin Signaling in Arabidopsis1[W] , 2006, Plant Physiology.

[15]  T. Asami,et al.  Inhibition of Brassinosteroid Biosynthesis by Either a dwarf4 Mutation or a Brassinosteroid Biosynthesis Inhibitor Rescues Defects in Tropic Responses of Hypocotyls in the Arabidopsis Mutant nonphototropic hypocotyl 41 , 2006, Plant Physiology.

[16]  W. G. Brenner,et al.  Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. , 2005, The Plant journal : for cell and molecular biology.

[17]  L. Lehle,et al.  The Auxin-induced Maize Gene ZmSAUR2 Encodes a Short-lived Nuclear Protein Expressed in Elongating Tissues* , 2003, Journal of Biological Chemistry.

[18]  Charlie Chang,et al.  Functional Genomic Analysis of the AUXIN RESPONSE FACTOR Gene Family Members in Arabidopsis thaliana: Unique and Overlapping Functions of ARF7 and ARF19w⃞ , 2005, The Plant Cell Online.

[19]  Irina Mitina,et al.  AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. , 2005, The Plant journal : for cell and molecular biology.

[20]  J. Ecker,et al.  HOOKLESS1, an Ethylene Response Gene, Is Required for Differential Cell Elongation in the Arabidopsis Hypocotyl , 1996, Cell.

[21]  H. Tsukaya,et al.  The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. , 2002, Plant & cell physiology.

[22]  G. Hagen,et al.  ARF1, a transcription factor that binds to auxin response elements. , 1997, Science.

[23]  J. Ecker,et al.  Functional Genomic Analysis of the AUXIN/INDOLE-3-ACETIC ACID Gene Family Members in Arabidopsis thaliana[W] , 2005, The Plant Cell Online.

[24]  Ian B. Jeffery,et al.  Comparison and evaluation of methods for generating differentially expressed gene lists from microarray data , 2006, BMC Bioinformatics.

[25]  J. Ward,et al.  BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. , 2005, The Plant journal : for cell and molecular biology.

[26]  M. May,et al.  Oxidative Stimulation of Glutathione Synthesis in Arabidopsis thaliana Suspension Cultures , 1993, Plant physiology.

[27]  Huai Wang,et al.  The Embryo MADS Domain Protein AGAMOUS-Like 15 Directly Regulates Expression of a Gene Encoding an Enzyme Involved in Gibberellin Metabolism , 2004, The Plant Cell Online.

[28]  G. Hagen,et al.  Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. , 1997, The Plant cell.

[29]  Valérie Laucou,et al.  Cytokinin-Deficient Transgenic Arabidopsis Plants Show Multiple Developmental Alterations Indicating Opposite Functions of Cytokinins in the Regulation of Shoot and Root Meristem Activity Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014928 , 2003, The Plant Cell Online.

[30]  A. Theologis,et al.  Early auxin-regulated polyadenylylated mRNA sequences in pea stem tissue. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[31]  S. Dorey,et al.  A pharmacological approach to test the diffusible signal activity of reactive oxygen intermediates in elicitor-treated tobacco leaves. , 2002, Plant & cell physiology.

[32]  Tom Beeckman,et al.  Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression , 2005, Development.

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

[34]  W. Longabaugh,et al.  Computational representation of developmental genetic regulatory networks. , 2005, Developmental biology.

[35]  B. Bartel,et al.  Auxin: regulation, action, and interaction. , 2005, Annals of botany.

[36]  J. Smith,et al.  Evidence that auxin promotes gibberellin A1 biosynthesis in pea. , 2000, The Plant journal : for cell and molecular biology.

[37]  I. Blilou,et al.  The PIN auxin efflux facilitators: evolutionary and functional perspectives. , 2005, Trends in plant science.

[38]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

[39]  D. Inzé,et al.  Cell Cycle Progression in the Pericycle Is Not Sufficient for SOLITARY ROOT/IAA14-Mediated Lateral Root Initiation in Arabidopsis thalianaw⃞ , 2005, The Plant Cell Online.

[40]  G. Hagen,et al.  Activation and repression of transcription by auxin-response factors. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[41]  A. Theologis,et al.  Unique and Overlapping Expression Patterns among the Arabidopsis 1-Amino-Cyclopropane-1-Carboxylate Synthase Gene Family Members1[w] , 2004, Plant Physiology.

[42]  Joseph R. Ecker,et al.  Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation , 2005, Development.

[43]  D. Inzé,et al.  Transcript profiling of early lateral root initiation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[44]  T. Guilfoyle,et al.  Rapid redistribution of auxin-regulated RNAs during gravitropism. , 1989, Science.

[45]  G. Jürgens,et al.  Funneling auxin action: specificity in signal transduction. , 2004, Current opinion in plant biology.

[46]  Christopher D Town,et al.  Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. , 2004, The Plant journal : for cell and molecular biology.

[47]  T. Vision,et al.  Contrasting Modes of Diversification in the Aux/IAA and ARF Gene Families1[w] , 2004, Plant Physiology.

[48]  T. Koshiba,et al.  The HAT2 gene, a member of the HD-Zip gene family, isolated as an auxin inducible gene by DNA microarray screening, affects auxin response in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[49]  G. Hagen,et al.  Auxin-responsive gene expression: genes, promoters and regulatory factors , 2002, Plant Molecular Biology.

[50]  P. Hooykaas.  Biochemistry and Molecular Biology of Plant Hormones , 1999 .

[51]  M. Uhlén,et al.  Assembly of a gene sequence tag microarray by reversible biotin-streptavidin capture for transcript analysis of Arabidopsis thaliana , 2005, BMC biotechnology.

[52]  T. Berleth,et al.  Responses of plant vascular systems to auxin transport inhibition. , 1999, Development.

[53]  Jennifer L. Nemhauser,et al.  Different Plant Hormones Regulate Similar Processes through Largely Nonoverlapping Transcriptional Responses , 2006, Cell.

[54]  Ana I. Caño-Delgado,et al.  BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis , 2004, Development.

[55]  Klaus Palme,et al.  Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis , 2002, Nature.

[56]  K. Dreher,et al.  The Arabidopsis Aux/IAA Protein Family Has Diversified in Degradation and Auxin Responsiveness[W] , 2006, The Plant Cell Online.

[57]  W. Haddon,et al.  Biochemical Diversity among the 1-Amino-cyclopropane-1-Carboxylate Synthase Isozymes Encoded by the Arabidopsis Gene Family* , 2003, Journal of Biological Chemistry.

[58]  Ross Ihaka,et al.  Gentleman R: R: A language for data analysis and graphics , 1996 .

[59]  Wolfgang Busch,et al.  WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators , 2005, Nature.

[60]  Stefan R. Henz,et al.  A gene expression map of Arabidopsis thaliana development , 2005, Nature Genetics.

[61]  T. Speed,et al.  Summaries of Affymetrix GeneChip probe level data. , 2003, Nucleic acids research.

[62]  Ottoline Leyser,et al.  Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins , 2001, Nature.

[63]  L. Sieburth,et al.  Auxin is required for leaf vein pattern in Arabidopsis. , 1999, Plant physiology.

[64]  Joseph M. Dale,et al.  Identification of inhibitors of auxin transcriptional activation by means of chemical genetics in Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[65]  Joseph R Ecker,et al.  NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. , 2005, The Plant journal : for cell and molecular biology.

[66]  Nicole K Clay,et al.  Arabidopsis thickvein Mutation Affects Vein Thickness and Organ Vascularization, and Resides in a Provascular Cell-Specific Spermine Synthase Involved in Vein Definition and in Polar Auxin Transport1 , 2005, Plant Physiology.

[67]  T. Steeves,et al.  Patterns in plant development: Subject index , 1972 .

[68]  K. Feldmann,et al.  The DWF4 Gene of Arabidopsis Encodes a Cytochrome P450 That Mediates Multiple 22α-Hydroxylation Steps in Brassinosteroid Biosynthesis , 1998, Plant Cell.

[69]  Klaus Palme,et al.  Auxin in action: signalling, transport and the control of plant growth and development , 2006, Nature Reviews Molecular Cell Biology.

[70]  O. Leyser,et al.  Rapid Degradation of Auxin/Indoleacetic Acid Proteins Requires Conserved Amino Acids of Domain II and Is Proteasome Dependent , 2001, The Plant Cell Online.

[71]  Ken-ichiro Hayashi,et al.  p-Chlorophenoxyisobutyric Acid Impairs Auxin Response in Arabidopsis Root1 , 2003, Plant Physiology.