AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis.

Catalase and hydrogen peroxide (H(2)O(2)) have been extensively studied for their roles in various stress responses. However, little is known about the triggering mechanisms for stress-induced catalase gene expression or about H(2)O(2) production as a stress signal. It is reported here that ABA-, drought-, and salt stress-induced gene expression of CAT1 catalase is mediated by AtMEK1, an Arabidopsis MAPK kinase, by triggering H(2)O(2) signal production. Both CAT1 expression and AtMEK1 activity were activated by ABA, drought, and salt stresses. The mek1 mutant totally blocked stress-induced CAT1 expression and, interestingly, stress-induced H(2)O(2) production was also blocked. Over-expression of AtMEK1 significantly promoted stress-induced CAT1 expression, and also promoted H(2)O(2) production. These results conclusively indicate that stress-induced CAT1 expression is mediated by AtMEK1 and, furthermore, that the triggering of H(2)O(2) production might be involved in this process, as further proved by the observation that CAT1 expression was induced by applied H(2)O(2.) Surprisingly, the signalling mechanisms for stress-induced gene expression of CAT2 and CAT3 were very different from that of CAT1. Except for drought stress, expression of CAT2 or CAT3 was also activated by salt stress or ABA treatment, and AtMEK1 was not proved to be involved in the drought-induced expression of CAT2 or CAT3. Further studies showed that stomatal movement was much less sensitive to ABA in AtMEK1 mutant (mek1), and over-expression of AtMEK1 in Arabidopsis increased plant resistance to drought or salt stress, which further demonstrated that AtMEK1 is a crucial mediator in plant stress signal transduction.

[1]  H. Hirt,et al.  Reactive oxygen species signaling in plants. , 2006, Antioxidants & redox signaling.

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

[3]  H. Kamada,et al.  A mitogen-activated protein kinase NtMPK4 activated by SIPKK is required for jasmonic acid signaling and involved in ozone tolerance via stomatal movement in tobacco. , 2005, Plant & cell physiology.

[4]  C. Foyer,et al.  Redox Homeostasis and Antioxidant Signaling: A Metabolic Interface between Stress Perception and Physiological Responses , 2005, The Plant Cell Online.

[5]  Andrea Pitzschke,et al.  Emerging MAP kinase pathways in plant stress signalling. , 2005, Trends in plant science.

[6]  C. R. McClung,et al.  The circadian clock gates expression of twoArabidopsis catalase genes to distinct and opposite circadian phases , 1996, Molecular and General Genetics MGG.

[7]  D. Inzé,et al.  Genome-Wide Analysis of Hydrogen Peroxide-Regulated Gene Expression in Arabidopsis Reveals a High Light-Induced Transcriptional Cluster Involved in Anthocyanin Biosynthesis , 2005 .

[8]  K. Shinozaki,et al.  The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. , 2004, Molecular cell.

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

[10]  J. Hancock,et al.  ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. , 2003, Journal of experimental botany.

[11]  J. Giraudat,et al.  Cloning and characterisation of MEK1, an Arabidopsis gene encoding a homologue of MAP kinase kinase , 1997, Plant Molecular Biology.

[12]  H. Hirt,et al.  REACTIVE OXYGEN SPECIES: Metabolism, , 2004 .

[13]  Simon Gilroy,et al.  Allelopathy and Exotic Plant Invasion: From Molecules and Genes to Species Interactions , 2003, Science.

[14]  M. Schmid,et al.  Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana , 2003, Science.

[15]  Jonathan D. G. Jones,et al.  Reactive oxygen species produced by NADPH oxidase regulate plant cell growth , 2003, Nature.

[16]  Jonathan D. G. Jones,et al.  Nicotiana benthamiana gp91phox Homologs NbrbohA and NbrbohB Participate in H2O2 Accumulation and Resistance to Phytophthora infestans Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008680. , 2003, The Plant Cell Online.

[17]  M. Cho,et al.  NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Hancock,et al.  Hydrogen peroxide and nitric oxide as signalling molecules in plants. , 2002, Journal of experimental botany.

[19]  T. Nanmori,et al.  Activation of AtMEK1, an Arabidopsis mitogen-activated protein kinase kinase, in vitro and in vivo: analysis of active mutants expressed in E. coli and generation of the active form in stress response in seedlings. , 2002, The Plant journal : for cell and molecular biology.

[20]  F. Ausubel,et al.  MAP kinase signalling cascade in Arabidopsis innate immunity , 2002, Nature.

[21]  D. Ren,et al.  Cell Death Mediated by MAPK Is Associated with Hydrogen Peroxide Production in Arabidopsis * , 2002, The Journal of Biological Chemistry.

[22]  Ronald V. Maier,et al.  Mitogen-activated protein kinases. , 2002, Critical care medicine.

[23]  R. L. Jones,et al.  Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. , 2008, The Plant journal : for cell and molecular biology.

[24]  D. Galbraith,et al.  Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. , 2001, Plant physiology.

[25]  Julian I. Schroeder,et al.  Guard cell abscisic acid signalling and engineering drought hardiness in plants , 2001, Nature.

[26]  J. J. Grant,et al.  Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. , 2000, The Plant journal : for cell and molecular biology.

[27]  Zhen-Ming Pei,et al.  Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells , 2000, Nature.

[28]  B. Ellis,et al.  Ozone treatment rapidly activates MAP kinase signalling in plants. , 2000, The Plant journal : for cell and molecular biology.

[29]  J. G. Scandalios,et al.  Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. , 2000, The Plant journal : for cell and molecular biology.

[30]  S. Luan,et al.  ATMPK4, an Arabidopsis homolog of mitogen-activated protein kinase, is activated in vitro by AtMEK1 through threonine phosphorylation. , 2000, Plant physiology.

[31]  G. Tena,et al.  Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[32]  E. Burnett,et al.  ABA activation of an MBP kinase in Pisum sativum epidermal peels correlates with stomatal responses to ABA. , 2000, Journal of experimental botany.

[33]  H. Hirt,et al.  An international conference with a high ambition , 2000 .

[34]  J. Hancock,et al.  H2O2 activates a MAP kinase-like enzyme in Arabidopsis thaliana suspension cultures , 1999 .

[35]  S. Assmann,et al.  Ozone inhibits guard cell K+ channels implicated in stomatal opening. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Ze'ev Ronai,et al.  Role of redox potential and reactive oxygen species in stress signaling , 1999, Oncogene.

[37]  S. Rhee Redox signaling: hydrogen peroxide as intracellular messenger , 1999, Experimental & Molecular Medicine.

[38]  A. Puga,et al.  Regulation of gene expression by reactive oxygen. , 1999, Annual review of pharmacology and toxicology.

[39]  H. Kamata,et al.  Redox regulation of cellular signalling. , 1999, Cellular signalling.

[40]  K. Irie,et al.  Isolation of ATMEKK1 (a MAP kinase kinase kinase)-interacting proteins and analysis of a MAP kinase cascade in Arabidopsis. , 1998, Biochemical and biophysical research communications.

[41]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[42]  Sutherland,et al.  Use of a new tetrazolium-based assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoospores of phytophthora parasitica var nicotianae , 1998, Plant physiology.

[43]  C. R. McClung,et al.  Intron loss and gain during evolution of the catalase gene family in angiosperms. , 1998, Genetics.

[44]  L. Bülow,et al.  Improving stress tolerance in plants by gene transfer , 1998 .

[45]  D Scheel,et al.  Receptor-mediated activation of a MAP kinase in pathogen defense of plants. , 1997, Science.

[46]  G. Paliyath,et al.  Changes in Activities of Antioxidant Enzymes and Their Relationship to Genetic and Paclobutrazol-Induced Chilling Tolerance of Maize Seedlings , 1997, Plant physiology.

[47]  H. Lander An essential role for free radicals and derived species in signal transduction , 1997, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[48]  Heribert Hirt,et al.  Multiple roles of MAP kinases in plant signal transduction , 1997 .

[49]  K. Shinozaki,et al.  Environmental stress response in plants: the role of mitogen-activated protein kinases. , 1997, Trends in biotechnology.

[50]  T. Abe [Calcium channels]. , 1997, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[51]  C. R. McClung,et al.  Catalase Is Encoded by a Multigene Family in Arabidopsis thaliana (L.) Heynh , 1996, Plant physiology.

[52]  A. Hetherington,et al.  Changes in Stomatal Behavior and Guard Cell Cytosolic Free Calcium in Response to Oxidative Stress , 1996, Plant physiology.

[53]  C. Foyer Oxygen processing in photosynthesis. , 1996, Biochemical Society transactions.

[54]  P. Low,et al.  The oxidative burst in plant defense: Function and signal transduction , 1996 .

[55]  D. Mount Reprogramming transcription , 1996, Nature.

[56]  V. Adler,et al.  UV Irradiation and Heat Shock Mediate JNK Activation via Alternate Pathways (*) , 1995, The Journal of Biological Chemistry.

[57]  J. Ryals,et al.  Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance , 1995 .

[58]  E. W. Orlandi,et al.  Active oxygen in plant pathogenesis. , 1995, Annual review of phytopathology.

[59]  Christine H. Foyer,et al.  Photooxidative stress in plants , 1994 .

[60]  Alex Levine,et al.  H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response , 1994, Cell.

[61]  D. Klessig,et al.  Salicylic acid, active oxygen species and systemic acquired resistance in plants. , 1994, Trends in cell biology.

[62]  C. R. McClung,et al.  Interactions between Light and the Circadian Clock in the Regulation of CAT2 Expression in Arabidopsis , 1994, Plant physiology.

[63]  A. Theologis,et al.  Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. , 1994, The Plant journal : for cell and molecular biology.

[64]  B. Glick,et al.  Methods in Plant Molecular Biology and Biotechnology , 1993 .

[65]  J. Thompson,et al.  Transient analysis of gene expression in plant cells. , 1993 .

[66]  K. Skriver,et al.  cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[67]  J. Fütterer,et al.  Positive and negative control of translation by the leader sequence of cauliflower mosaic virus pregenomic 35S RNA. , 1990, The EMBO journal.

[68]  Y. Arai,et al.  An improved assay for β-glucuronidase in transformed cells: methanol almost completely suppresses a putative endogenous β-glucuronidase activity. , 1990 .

[69]  谢成颂,et al.  烟草黑胫病菌(Phytophthora parasitica var, nicotianae)... , 1989 .

[70]  I. Fridovich,et al.  Catalases--with and without heme. , 1988, Basic life sciences.

[71]  John F. Ward,et al.  Oxygen Radicals in Biology and Medicine , 1988, Basic Life Sciences.