Arabidopsis Cys2/His2 Zinc-Finger Proteins AZF1 and AZF2 Negatively Regulate Abscisic Acid-Repressive and Auxin-Inducible Genes under Abiotic Stress Conditions1[W][OA]

In plants, abiotic stresses induce various physiological changes and growth inhibition that result in adaptive responses to these stresses. However, little is known about how such stresses cause plant growth inhibition. Many genes have been reported to be repressed in plants under abiotic stress conditions. ZPT2 (for petunia [Petunia hybrida] zinc-finger protein 2)-related proteins with two Cys2/His2-type zinc-finger motifs and an ethylene-responsive element binding factor-associated amphiphilic repression motif are thought to function as transcriptional repressors. To characterize the roles of this type of transcriptional repressor under abiotic stress conditions, we analyzed the functions of two Arabidopsis (Arabidopsis thaliana) ZPT2-related genes that were induced by osmotic stress and abscisic acid: AZF1 (for Arabidopsis zinc-finger protein 1) and AZF2. The nuclear localization of these two proteins was observed in the roots under control conditions, and the accumulation of AZF2 was clearly detected in the nuclei of leaf cells under stress conditions. Transgenic plants overexpressing AZF1 and AZF2 were generated using stress-responsive promoters or the GVG chemical induction system. The overexpression of these genes caused severe damage to plant growth and viability. Transcriptome analyses of the transgenic plants demonstrated that AZF1 and AZF2 repressed various genes that were down-regulated by osmotic stress and abscisic acid treatment. Moreover, many auxin-responsive genes were found to be commonly down-regulated in the transgenic plants. Gel mobility shift assays revealed that both the AZF1 and AZF2 proteins bound to the promoter regions of these down-regulated genes. These results indicate that AZF1 and AZF2 function as transcriptional repressors involved in the inhibition of plant growth under abiotic stress conditions.

[1]  C. Perrot-Rechenmann,et al.  Recent progress in auxin biology. , 2010, Comptes rendus biologies.

[2]  D. Inzé,et al.  NINJA connects the co-repressor TOPLESS to jasmonate signalling , 2010, Nature.

[3]  K. Shinozaki,et al.  AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. , 2010, The Plant journal : for cell and molecular biology.

[4]  K. Shinozaki,et al.  Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. , 2009, Plant & cell physiology.

[5]  S. Barak,et al.  Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots , 2009, Journal of experimental botany.

[6]  K. Shinozaki,et al.  Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. , 2009, Plant & cell physiology.

[7]  Kazuo Shinozaki,et al.  Arabidopsis DREB2A-Interacting Proteins Function as RING E3 Ligases and Negatively Regulate Plant Drought Stress–Responsive Gene Expression[W] , 2008, The Plant Cell Online.

[8]  Ben Scheres,et al.  Auxin: the looping star in plant development. , 2008, Annual review of plant biology.

[9]  Joanne Chory,et al.  Rapid Synthesis of Auxin via a New Tryptophan-Dependent Pathway Is Required for Shade Avoidance in Plants , 2008, Cell.

[10]  J. Long,et al.  TOPLESS Mediates Auxin-Dependent Transcriptional Repression During Arabidopsis Embryogenesis , 2008, Science.

[11]  Klaus Palme,et al.  Comprehensive transcriptome analysis of auxin responses in Arabidopsis. , 2008, Molecular plant.

[12]  R. Mittler,et al.  The zinc finger network of plants , 2008, Cellular and Molecular Life Sciences.

[13]  R. Mittler,et al.  The EAR-motif of the Cys2/His2-type Zinc Finger Protein Zat7 Plays a Key Role in the Defense Response of Arabidopsis to Salinity Stress* , 2007, Journal of Biological Chemistry.

[14]  K. Palme,et al.  Stress-induced morphogenic responses: growing out of trouble? , 2007, Trends in plant science.

[15]  Jian-Kang Zhu,et al.  Gain‐ and loss‐of‐function mutations in Zat10 enhance the tolerance of plants to abiotic stress , 2006, FEBS letters.

[16]  Dirk Inzé,et al.  A novel role for abscisic acid emerges from underground. , 2006, Trends in plant science.

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

[18]  Kazuo Shinozaki,et al.  Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. , 2006, Annual review of plant biology.

[19]  K. Kazan.  Negative regulation of defence and stress genes by EAR-motif-containing repressors. , 2006, Trends in plant science.

[20]  T. Sakurai,et al.  Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray , 2004, Plant Molecular Biology.

[21]  Kazuo Shinozaki,et al.  Arabidopsis Cys2/His2-Type Zinc-Finger Proteins Function as Transcription Repressors under Drought, Cold, and High-Salinity Stress Conditions1 , 2004, Plant Physiology.

[22]  Heiko Schoof,et al.  Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome , 2004, BMC Genomics.

[23]  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.

[24]  N. Chua,et al.  The Arabidopsis Auxin-Inducible Gene ARGOS Controls Lateral Organ Size Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.013557. , 2003, The Plant Cell Online.

[25]  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.

[26]  Michele Morgante,et al.  Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant , 2002, Journal of Cell Science.

[27]  Hur-Song Chang,et al.  Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress1,212 , 2002, Plant Physiology.

[28]  S. Fujioka,et al.  Microarray Analysis of Brassinosteroid-Regulated Genes in Arabidopsis , 2002, Plant Physiology.

[29]  K. Akiyama,et al.  Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. , 2002, The Plant journal : for cell and molecular biology.

[30]  M. Ohta,et al.  LOS2, a genetic locus required for cold‐responsive gene transcription encodes a bi‐functional enolase , 2002, The EMBO journal.

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

[32]  R. Finkelstein,et al.  Abscisic Acid Signaling in Seeds and Seedlings Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010441. , 2002, The Plant Cell Online.

[33]  Hur-Song Chang,et al.  Expression Profile Matrix of Arabidopsis Transcription Factor Genes Suggests Their Putative Functions in Response to Environmental Stresses , 2002, The Plant Cell Online.

[34]  G. Hagen,et al.  Auxin Response Factors , 2001, Journal of Plant Growth Regulation.

[35]  K. Hiratsu,et al.  Repression Domains of Class II ERF Transcriptional Repressors Share an Essential Motif for Active Repression , 2001, The Plant Cell Online.

[36]  P. Hasegawa,et al.  Genes that are uniquely stress regulated in salt overly sensitive (sos) mutants. , 2001, Plant physiology.

[37]  P. Wright,et al.  Zinc finger proteins: new insights into structural and functional diversity. , 2001, Current opinion in structural biology.

[38]  M. Iwabuchi,et al.  Expression of a subset of the Arabidopsis Cys(2)/His(2)-type zinc-finger protein gene family under water stress. , 2000, Gene.

[39]  H. Takatsuji,et al.  Zinc-finger proteins: the classical zinc finger emerges in contemporary plant science , 1999, Plant Molecular Biology.

[40]  P. Busk,et al.  Regulation of abscisic acid-induced transcription , 1998, Plant Molecular Biology.

[41]  J. Giraudat,et al.  ABSCISIC ACID SIGNAL TRANSDUCTION. , 1998, Annual review of plant physiology and plant molecular biology.

[42]  N. Chua,et al.  A glucocorticoid-mediated transcriptional induction system in transgenic plants. , 1997, The Plant journal : for cell and molecular biology.

[43]  M. Cyert,et al.  Two Classes of Plant cDNA Clones Differentially Complement Yeast Calcineurin Mutants and Increase Salt Tolerance of Wild-type Yeast* , 1996, The Journal of Biological Chemistry.

[44]  A Klug,et al.  Zinc fingers , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[45]  K. Shinozaki,et al.  A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. , 1994, The Plant cell.

[46]  P. Benfey,et al.  Characterization of a zinc finger DNA‐binding protein expressed specifically in Petunia petals and seedlings. , 1992, The EMBO journal.

[47]  G. Hagen,et al.  Tissue-specific and organ-specific expression of soybean auxin-responsive transcripts GH3 and SAURs. , 1991, The Plant cell.

[48]  J. Tom,et al.  Tissue-Specific and Organ-Specific Expression of Soybean Auxin-Responsive Transcripts GH 3 and SAURs , 2002 .

[49]  C. Pabo,et al.  Design and selection of novel Cys2His2 zinc finger proteins. , 2001, Annual review of biochemistry.

[50]  K. Yamaguchi-Shinozaki,et al.  Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. , 1999, Nature biotechnology.

[51]  G. Pelletier,et al.  In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. , 1998, Methods in molecular biology.

[52]  A. Sakamoto,et al.  Cys2/His2 zinc-finger protein family of petunia: evolution and general mechanism of target-sequence recognition. , 1998, Nucleic acids research.

[53]  M. Ohta,et al.  LOS 2 , a genetic locus required for cold-responsive gene transcription encodes a bifunctional enolase , 2022 .