The HSF-like Transcription Factor TBF1 Is a Major Molecular Switch for Plant Growth-to-Defense Transition

BACKGROUND Induction of plant immune responses involves significant transcription reprogramming that prioritizes defense over growth-related cellular functions. Despite intensive forward genetic screens and genome-wide expression-profiling studies, a limited number of transcription factors have been found that regulate this transition. RESULTS Using the endoplasmic-reticulum-resident genes required for antimicrobial protein secretion as markers, we identified a heat-shock factor-like transcription factor that specifically binds to the TL1 (GAAGAAGAA) cis element required for the induction of these genes. Surprisingly, plants lacking this TL1-binding factor, TBF1, respond normally to heat stress but are compromised in immune responses induced by salicylic acid and by microbe-associated molecular pattern, elf18. Genome-wide expression profiling indicates that TBF1 plays a key role in the growth-to-defense transition. Moreover, the expression of TBF1 itself is tightly regulated at both the transcriptional and translational levels. Two upstream open reading frames encoding multiple aromatic amino acids were found 5' of the translation initiation codon of TBF1 and shown to affect its translation. CONCLUSIONS Through this unique regulatory mechanism, TBF1 can sense the metabolic changes upon pathogen invasion and trigger the specific transcriptional reprogramming through its target genes expression.

[1]  P. Heifetz,et al.  Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. , 1998, The Plant journal : for cell and molecular biology.

[2]  Xinnian Dong,et al.  Nuclear Localization of NPR1 Is Required for Activation of PR Gene Expression , 2000, Plant Cell.

[3]  T. Salem,et al.  Plant class B HSFs inhibit transcription and exhibit affinity for TFIIB and TBP , 2004, Plant Molecular Biology.

[4]  M. Waltham,et al.  Variants of human dihydrofolate reductase with substitutions at leucine-22: effect on catalytic and inhibitor binding properties. , 1996, Molecular pharmacology.

[5]  Nicolas Guex,et al.  Natural variation of potato allene oxide synthase 2 causes differential levels of jasmonates and pathogen resistance in Arabidopsis , 2008, Planta.

[6]  Andrew J. Heidel,et al.  Fitness Costs of Mutations Affecting the Systemic Acquired Resistance Pathway in Arabidopsis thaliana , 2004, Genetics.

[7]  Karolina M. Pajerowska-Mukhtar,et al.  Receptor quality control in the endoplasmic reticulum for plant innate immunity , 2009, The EMBO journal.

[8]  E. Westhof,et al.  Binding of tobramycin leads to conformational changes in yeast tRNAAsp and inhibition of aminoacylation , 2002, The EMBO journal.

[9]  A. Hinnebusch,et al.  Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-binding domain. , 2000, Molecular cell.

[10]  S. Somerville,et al.  Genome-Wide Expression Profiling Arabidopsis at the Stage of Golovinomyces cichoracearum Haustorium Formation1[W][OA] , 2008, Plant Physiology.

[11]  Uwe Conrath,et al.  Systemic Acquired Resistance , 2006, Plant signaling & behavior.

[12]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[13]  P. Schulze-Lefert,et al.  Secretory Pathways in Plant Immune Responses1 , 2008, Plant Physiology.

[14]  T. Boller,et al.  Perception of the Bacterial PAMP EF-Tu by the Receptor EFR Restricts Agrobacterium-Mediated Transformation , 2006, Cell.

[15]  Klaus-Dieter Scharf,et al.  Complexity of the heat stress response in plants. , 2007, Current opinion in plant biology.

[16]  Dong Wang,et al.  Induction of Protein Secretory Pathway Is Required for Systemic Acquired Resistance , 2005, Science.

[17]  F. Sicheri,et al.  Conserved Intermolecular Salt Bridge Required for Activation of Protein Kinases PKR, GCN2, and PERK* , 2007, Journal of Biological Chemistry.

[18]  C. Zipfel,et al.  Control of the pattern‐recognition receptor EFR by an ER protein complex in plant immunity , 2009, The EMBO journal.

[19]  T. Holton,et al.  Genetics and Biochemistry of Anthocyanin Biosynthesis. , 1995, The Plant cell.

[20]  Kapil Bharti,et al.  Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors , 2004, Journal of Biosciences.

[21]  A. Hinnebusch,et al.  cis-acting sequences involved in the translational control of GCN4 expression. , 1990, Biochimica et biophysica acta.

[22]  T. Eulgem,et al.  The WRKY superfamily of plant transcription factors. , 2000, Trends in plant science.

[23]  Celine A. Hayden,et al.  Identification of novel conserved peptide uORF homology groups in Arabidopsis and rice reveals ancient eukaryotic origin of select groups and preferential association with transcription factor-encoding genes , 2007, BMC Biology.

[24]  Paul Schulze-Lefert,et al.  SnapShot: Plant Immune Response Pathways , 2009, Cell.

[25]  K. Scharf,et al.  Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? , 2001, Cell stress & chaperones.

[26]  N. Hayashi,et al.  Role of OsNPR1 in rice defense program as revealed by genome-wide expression analysis , 2010, Plant Molecular Biology.

[27]  K. Hinderhofer,et al.  HSF3, a new heat shock factor from Arabidopsis thaliana, derepresses the heat shock response and confers thermotolerance when overexpressed in transgenic plants , 1998, Molecular and General Genetics MGG.

[28]  A. Loraine,et al.  A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity , 2010, Proceedings of the National Academy of Sciences.

[29]  Stanley Fields,et al.  A yeast sensor of ligand binding , 2001, Nature Biotechnology.

[30]  A. Hinnebusch.  Translational regulation of GCN4 and the general amino acid control of yeast. , 2005, Annual review of microbiology.

[31]  T. Boller,et al.  Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele , 2009, Proceedings of the National Academy of Sciences.

[32]  Jonathan D. G. Jones,et al.  Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR , 2009, Proceedings of the National Academy of Sciences.

[33]  W. Busch,et al.  Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. , 2009, Molecular plant.

[34]  J. Glazebrook,et al.  Network Properties of Robust Immunity in Plants , 2009, PLoS genetics.

[35]  Jeffery L Dangl,et al.  Arabidopsis and the plant immune system. , 2010, The Plant journal : for cell and molecular biology.

[36]  M. Kozak,et al.  An analysis of vertebrate mRNA sequences: intimations of translational control , 1991, The Journal of cell biology.

[37]  Xin Li,et al.  Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[38]  K. Scharf,et al.  Plants contain a novel multi-member class of heat shock factors without transcriptional activator potential , 2000, Plant Molecular Biology.

[39]  Wolfgang Busch,et al.  Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[40]  C. Queitsch,et al.  Heat stress transcription factors from tomato can functionally replace HSF1 in the yeast Saccharomyces cerevisiaet , 1997, Molecular and General Genetics MGG.

[41]  U. Grossniklaus,et al.  A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta[w] , 2003, Plant Physiology.

[42]  Yunde Zhao.  Auxin biosynthesis and its role in plant development. , 2010, Annual review of plant biology.

[43]  Shui Wang,et al.  DNA repair proteins are directly involved in regulation of gene expression during plant immune response. , 2011, Cell host & microbe.

[44]  J. Deragon,et al.  Arabidopsis eIF2α kinase GCN2 is essential for growth in stress conditions and is activated by wounding , 2008, BMC Plant Biology.

[45]  A. Hinnebusch,et al.  Structural Basis for Autoinhibition and Mutational Activation of Eukaryotic Initiation Factor 2α Protein Kinase GCN2*[boxs] , 2005, Journal of Biological Chemistry.