A stele-enriched gene regulatory network in the Arabidopsis root

Tightly controlled gene expression is a hallmark of multicellular development and is accomplished by transcription factors (TFs) and microRNAs (miRNAs). Although many studies have focused on identifying downstream targets of these molecules, less is known about the factors that regulate their differential expression. We used data from high spatial resolution gene expression experiments and yeast one‐hybrid (Y1H) and two‐hybrid (Y2H) assays to delineate a subset of interactions occurring within a gene regulatory network (GRN) that determines tissue‐specific TF and miRNA expression in plants. We find that upstream TFs are expressed in more diverse cell types than their targets and that promoters that are bound by a relatively large number of TFs correspond to key developmental regulators. The regulatory consequence of many TFs for their target was experimentally determined using genetic analysis. Remarkably, molecular phenotypes were identified for 65% of the TFs, but morphological phenotypes were associated with only 16%. This indicates that the GRN is robust, and that gene expression changes may be canalized or buffered.

[1]  Lynn Doucette-Stamm,et al.  A C . elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity , 2008 .

[2]  Reynaldo Sequerra,et al.  Functional modularity of nuclear hormone receptors in a Caenorhabditis elegans metabolic gene regulatory network , 2010, Molecular systems biology.

[3]  M. Vidal,et al.  High-throughput yeast two-hybrid assays for large-scale protein interaction mapping. , 2001, Methods.

[4]  C. Waddington Canalization of Development and the Inheritance of Acquired Characters , 1942, Nature.

[5]  Daniel L. Mace,et al.  A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns , 2007, Science.

[6]  A. J. Walhout,et al.  Gateway-compatible yeast one-hybrid screens. , 2006, CSH protocols.

[7]  Wolfgang Busch,et al.  Omics meet networks - using systems approaches to infer regulatory networks in plants. , 2010, Current opinion in plant biology.

[8]  Saranyan K. Palaniswamy,et al.  AGRIS and AtRegNet. A Platform to Link cis-Regulatory Elements and Transcription Factors into Regulatory Networks1[W][OA] , 2006, Plant Physiology.

[9]  P. Farnham Insights from genomic profiling of transcription factors , 2009, Nature Reviews Genetics.

[10]  V. Ambros,et al.  Genome-scale spatiotemporal analysis of Caenorhabditis elegans microRNA promoter activity. , 2008, Genome research.

[11]  F. Ariel,et al.  Transcriptional control of a plant stem cell niche. , 2010, Developmental cell.

[12]  Queenie K.-G. Tan,et al.  The Arabidopsis Zinc Finger-Homeodomain Genes Encode Proteins with Unique Biochemical Properties That Are Coordinately Expressed during Floral Development1 , 2006, Plant Physiology.

[13]  Eric H Davidson,et al.  Gene regulatory network subcircuit controlling a dynamic spatial pattern of signaling in the sea urchin embryo , 2008, Proceedings of the National Academy of Sciences.

[14]  S. Kauppinen,et al.  Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. , 2006, The Plant journal : for cell and molecular biology.

[15]  Bernd Sturmfels,et al.  Reconstructing spatiotemporal gene expression data from partial observations , 2009, Bioinform..

[16]  Mark Gerstein,et al.  Target hub proteins serve as master regulators of development in yeast. , 2006, Genes & development.

[17]  P. Benfey,et al.  Whole-Genome Analysis of the SHORT-ROOT Developmental Pathway in Arabidopsis , 2006, PLoS biology.

[18]  Sjef Smeekens,et al.  Two-hybrid protein-protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. , 2006, The Plant journal : for cell and molecular biology.

[19]  M. Vidal,et al.  A gateway-compatible yeast one-hybrid system. , 2004, Genome research.

[20]  Teva Vernoux,et al.  An Evolutionarily Conserved Mechanism Delimiting SHR Movement Defines a Single Layer of Endodermis in Plants , 2007, Science.

[21]  Albert-László Barabási,et al.  Transcription factor modularity in a gene-centered C. elegans core neuronal protein-DNA interaction network. , 2007, Genome research.

[22]  Miroslav Strnad,et al.  DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[23]  Lynn Doucette-Stamm,et al.  Matrix and Steiner-triple-system smart pooling assays for high-performance transcription regulatory network mapping , 2007, Nature Methods.

[24]  Tal Nawy,et al.  Transcriptional Profile of the Arabidopsis Root Quiescent Centerw⃞ , 2005, The Plant Cell Online.

[25]  Uwe Ohler,et al.  Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[26]  D. W. Knowles,et al.  Transcription Factors Bind Thousands of Active and Inactive Regions in the Drosophila Blastoderm , 2008, PLoS biology.

[27]  V. Ambros,et al.  The FLYWCH transcription factors FLH-1, FLH-2, and FLH-3 repress embryonic expression of microRNA genes in C. elegans. , 2008, Genes & development.

[28]  Christian A. Grove,et al.  A Gene-Centered C. elegans Protein-DNA Interaction Network , 2006, Cell.