An Arabidopsis Gene Regulatory Network for Secondary Cell Wall Synthesis

The plant cell wall is an important factor for determining cell shape, function and response to the environment. Secondary cell walls, such as those found in xylem, are composed of cellulose, hemicelluloses and lignin and account for the bulk of plant biomass. The coordination between transcriptional regulation of synthesis for each polymer is complex and vital to cell function. A regulatory hierarchy of developmental switches has been proposed, although the full complement of regulators remains unknown. Here we present a protein–DNA network between Arabidopsis thaliana transcription factors and secondary cell wall metabolic genes with gene expression regulated by a series of feed-forward loops. This model allowed us to develop and validate new hypotheses about secondary wall gene regulation under abiotic stress. Distinct stresses are able to perturb targeted genes to potentially promote functional adaptation. These interactions will serve as a foundation for understanding the regulation of a complex, integral plant component.

[1]  Michael F. Covington,et al.  Mechanical Stress Induces Biotic and Abiotic Stress Responses via a Novel cis-Element , 2007, PLoS genetics.

[2]  Ralf Zimmer,et al.  Inferring gene regulatory networks by ANOVA , 2012, Bioinform..

[3]  S. D. de Jager,et al.  © 2001 Kluwer Academic Publishers. Printed in the Netherlands. , 2000 .

[4]  D. Baulcombe,et al.  An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. , 2003, The Plant journal : for cell and molecular biology.

[5]  G. Coruzzi,et al.  Cell-specific nitrogen responses mediate developmental plasticity , 2008, Proceedings of the National Academy of Sciences.

[6]  Royston Goodacre,et al.  Identification of Novel Genes in Arabidopsis Involved in Secondary Cell Wall Formation Using Expression Profiling and Reverse Genetics , 2005, The Plant Cell Online.

[7]  R. Zhong,et al.  MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. , 2012, Plant & cell physiology.

[8]  Ghislain Breton,et al.  A Functional Genomics Approach Reveals CHE as a Component of the Arabidopsis Circadian Clock , 2009, Science.

[9]  Hunseung Kang,et al.  Identification of direct targets of transcription factor MYB46 provides insights into the transcriptional regulation of secondary wall biosynthesis , 2014, Plant Molecular Biology.

[10]  Steve A. Kay,et al.  The ELF4-ELF3-LUX Complex Links the Circadian Clock to Diurnal Control of Hypocotyl Growth , 2011, Nature.

[11]  Neil D. Lawrence,et al.  puma: a Bioconductor package for propagating uncertainty in microarray analysis , 2009, BMC Bioinformatics.

[12]  T. Demura,et al.  VND-INTERACTING2, a NAC Domain Transcription Factor, Negatively Regulates Xylem Vessel Formation in Arabidopsis[W][OA] , 2010, Plant Cell.

[13]  T. Demura,et al.  TERE; a novel cis-element responsible for a coordinated expression of genes related to programmed cell death and secondary wall formation during differentiation of tracheary elements. , 2007, The Plant journal : for cell and molecular biology.

[14]  Xing Wang Deng,et al.  Genome-Wide ORFeome Cloning and Analysis of Arabidopsis Transcription Factor Genes1[w] , 2004, Plant Physiology.

[15]  P. Geurts,et al.  Inferring Regulatory Networks from Expression Data Using Tree-Based Methods , 2010, PloS one.

[16]  C. Bergounioux,et al.  The E2F Family of Transcription Factors from Arabidopsis thaliana , 2002, The Journal of Biological Chemistry.

[17]  Beverly A. Underwood,et al.  Simultaneous high-throughput recombinational cloning of open reading frames in closed and open configurations. , 2006, Plant biotechnology journal.

[18]  Doreen Ware,et al.  Enhanced Y1H assays for Arabidopsis , 2011, Nature Methods.

[19]  S. Dinesh-Kumar,et al.  Molecular Chaperone Hsp90 Associates with Resistance Protein N and Its Signaling Proteins SGT1 and Rar1 to Modulate an Innate Immune Response in Plants* , 2004, Journal of Biological Chemistry.

[20]  D. Updegraff Semimicro determination of cellulose in biological materials. , 1969, Analytical biochemistry.

[21]  Jean-Philippe Vert,et al.  SIRENE: supervised inference of regulatory networks , 2008, ECCB.

[22]  J. Bowman,et al.  Roles for Class III HD-Zip and KANADI Genes in Arabidopsis Root Development1 , 2004, Plant Physiology.

[23]  Jungmook Kim,et al.  MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[24]  S. D. de Jager,et al.  Dissecting regulatory pathways of G1/S control in Arabidopsis: common and distinct targets of CYCD3;1, E2Fa and E2Fc , 2009, Plant Molecular Biology.

[25]  R. Zhong,et al.  A Battery of Transcription Factors Involved in the Regulation of Secondary Cell Wall Biosynthesis in Arabidopsis , 2008, The Plant Cell Online.

[26]  C. Gutiérrez,et al.  The E2FC-DPB Transcription Factor Controls Cell Division, Endoreplication and Lateral Root Formation in a SCFSKP2A- Dependent Manner , 2007, Plant signaling & behavior.

[27]  K. Shinozaki,et al.  The NAC Transcription Factors NST1 and NST2 of Arabidopsis Regulate Secondary Wall Thickenings and Are Required for Anther Dehiscencew⃞ , 2005, The Plant Cell Online.

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

[29]  T. Demura,et al.  VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. , 2011, The Plant journal : for cell and molecular biology.

[30]  Jean-Philippe Vert,et al.  TIGRESS: Trustful Inference of Gene REgulation using Stability Selection , 2012, BMC Systems Biology.

[31]  S. Kosugi,et al.  Interaction of the Arabidopsis E2F and DP Proteins Confers Their Concomitant Nuclear Translocation and Transactivation , 2002, Plant Physiology.

[32]  P. Benfey,et al.  Cell identity regulators link development and stress responses in the Arabidopsis root. , 2011, Developmental cell.

[33]  Sebastian E Ahnert,et al.  Power graph compression reveals dominant relationships in genetic transcription networks. , 2013, Molecular bioSystems.

[34]  Albertha J. M. Walhout,et al.  What does biologically meaningful mean? A perspective on gene regulatory network validation , 2011, Genome Biology.

[35]  Molly Megraw,et al.  A stele-enriched gene regulatory network in the Arabidopsis root , 2011, Molecular systems biology.

[36]  R. Zhong,et al.  MYB58 and MYB63 Are Transcriptional Activators of the Lignin Biosynthetic Pathway during Secondary Cell Wall Formation in Arabidopsis[C][W] , 2009, The Plant Cell Online.

[37]  C. Gutiérrez,et al.  Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light. , 2002, The Plant cell.

[38]  E. H. Melvin,et al.  Determination of Dextran with Anthrone , 1953 .

[39]  Richard Bonneau,et al.  DREAM4: Combining Genetic and Dynamic Information to Identify Biological Networks and Dynamical Models , 2010, PloS one.

[40]  L. De Veylder,et al.  The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. , 2011, The Plant journal : for cell and molecular biology.

[41]  C. Gutiérrez,et al.  The Balance between Cell Division and Endoreplication Depends on E2FC-DPB, Transcription Factors Regulated by the Ubiquitin-SCFSKP2A Pathway in Arabidopsis[W] , 2006, The Plant Cell Online.

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

[43]  T. Demura,et al.  VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 Effectively Induce Transdifferentiation into Xylem Vessel Elements under Control of an Induction System1[W] , 2010, Plant Physiology.

[44]  Kyung-Hwan Han,et al.  Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis , 2012, Plant Molecular Biology.

[45]  Tetsuro Mimura,et al.  Transcription switches for protoxylem and metaxylem vessel formation. , 2005, Genes & development.

[46]  Imre,et al.  REGIA, An EU Project on Functional Genomics of Transcription Factors From Arabidopsis Thaliana , 2002, Comparative and functional genomics.

[47]  A. Myburg,et al.  Navigating the transcriptional roadmap regulating plant secondary cell wall deposition , 2013, Front. Plant Sci..

[48]  M. Barton,et al.  A Feedback Regulatory Module Formed by LITTLE ZIPPER and HD-ZIPIII Genes[W][OA] , 2007, The Plant Cell Online.

[49]  H. Fukuda,et al.  Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 Directly Regulates the Genes That Govern Programmed Cell Death and Secondary Wall Formation during Xylem Differentiation[C][W] , 2010, Plant Cell.

[50]  Ykä Helariutta,et al.  Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate , 2010, Nature.

[51]  Staffan Persson,et al.  Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Diogo M. Camacho,et al.  Wisdom of crowds for robust gene network inference , 2012, Nature Methods.

[53]  Daniel L. Mace,et al.  Cell Identity Mediates the Response of Arabidopsis Roots to Abiotic Stress , 2008, Science.