NAC proteins: regulation and role in stress tolerance.

The plant-specific NAC (NAM, ATAF1,2 and CUC2) proteins constitute a major transcription factor family renowned for their roles in several developmental programs. Despite their highly conserved DNA-binding domains, their remarkable diversification across plants reflects their numerous functions. Lately, they have received much attention as regulators in various stress signaling pathways which may include interplay of phytohormones. This review summarizes the recent progress in research on NACs highlighting the proteins' potential for engineering stress tolerance against various abiotic and biotic challenges. We discuss regulatory components and targets of NAC proteins in the context of their prospective role for crop improvement strategies via biotechnological intervention.

[1]  S. Shigeoka,et al.  Identification of recognition sequence of ANAC078 protein by the cyclic amplification and selection of targets technique , 2010, Plant signaling & behavior.

[2]  Chung-Mo Park,et al.  Signaling linkage between environmental stress resistance and leaf senescence in Arabidopsis , 2011, Plant signaling & behavior.

[3]  M. K. Jensen,et al.  The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signalling. , 2010, The Biochemical journal.

[4]  Biao Ma,et al.  Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. , 2011, The Plant journal : for cell and molecular biology.

[5]  C. Koncz,et al.  NAC domain transcription factor ATAF1 interacts with SNF1-related kinases and silencing of its subfamily causes severe developmental defects in Arabidopsis , 2009 .

[6]  A. Parida,et al.  Transcript level characterization of a cDNA encoding stress regulated NAC transcription factor in the mangrove plant Avicennia marina. , 2008, Plant physiology and biochemistry : PPB.

[7]  Mathew G. Lewsey,et al.  Symptom induction and RNA silencing suppression by the cucumber mosaic virus 2b protein , 2010, Plant signaling & behavior.

[8]  R. Dixon,et al.  A Bioinformatic Analysis of NAC Genes for Plant Cell Wall Development in Relation to Lignocellulosic Bioenergy Production , 2009, BioEnergy Research.

[9]  Q. Xie,et al.  Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses , 2008, Cell Research.

[10]  K. Shinozaki,et al.  Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach , 2010, GM crops.

[11]  M. K. Jensen,et al.  Interactions between plant RING-H2 and plant-specific NAC (NAM/ATAF1/2/CUC2) proteins: RING-H2 molecular specificity and cellular localization. , 2003, The Biochemical journal.

[12]  Randeep Rakwal,et al.  The NAC transcription factor RIM1 of rice is a new regulator of jasmonate signaling. , 2010, The Plant journal : for cell and molecular biology.

[13]  Chung-Mo Park,et al.  A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. , 2008, The Plant journal : for cell and molecular biology.

[14]  P. A. Reis,et al.  Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. , 2009, Gene.

[15]  Sang Yeol Lee,et al.  Identification of a Calmodulin-binding NAC Protein as a Transcriptional Repressor in Arabidopsis* , 2007, Journal of Biological Chemistry.

[16]  S. Chen,et al.  Plant NAC-type transcription factor proteins contain a NARD domain for repression of transcriptional activation , 2010, Planta.

[17]  Gunnar Rätsch,et al.  Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. , 2009, The Plant journal : for cell and molecular biology.

[18]  Tao Ren,et al.  The nuclear localization of the Arabidopsis transcription factor TIP is blocked by its interaction with the coat protein of Turnip crinkle virus. , 2005, Virology.

[19]  Sun-Young Kim,et al.  Regulation of leaf senescence by NTL9-mediated osmotic stress signaling in Arabidopsis. , 2008, Molecules and cells.

[20]  S. Mori,et al.  A Novel NAC Transcription Factor, IDEF2, That Recognizes the Iron Deficiency-responsive Element 2 Regulates the Genes Involved in Iron Homeostasis in Plants* , 2008, Journal of Biological Chemistry.

[21]  K. Turksen,et al.  Isolation and characterization , 2006 .

[22]  A. Kamei,et al.  Analysis of gene expression profiles in Arabidopsis salt overly sensitive mutants sos 2-1 and sos 3-1 , 2022 .

[23]  Youn-sung Kim,et al.  Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation , 2006, Nucleic acids research.

[24]  Sun-Young Kim,et al.  A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis , 2007, Planta.

[25]  Jianhua Zhu,et al.  Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. , 2012, Biochimica et biophysica acta.

[26]  You-Liang Peng,et al.  Rice gene OsNAC19 encodes a novel NAC-domain transcription factor and responds to infection by Magnaporthe grisea , 2007 .

[27]  Kazuo Shinozaki,et al.  Genome-Wide Survey and Expression Analysis of the Plant-Specific NAC Transcription Factor Family in Soybean During Development and Dehydration Stress , 2011, DNA research : an international journal for rapid publication of reports on genes and genomes.

[28]  K. Shinozaki,et al.  Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. , 2007, The Plant journal : for cell and molecular biology.

[29]  F. Qu,et al.  HRT Gene Function Requires Interaction between a NAC Protein and Viral Capsid Protein to Confer Resistance to Turnip Crinkle Virus , 2000, Plant Cell.

[30]  Qi Xie,et al.  Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses , 2009, Cell Research.

[31]  G. Martin,et al.  Comprehensive transcript profiling of Pto- and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. , 2002, The Plant journal : for cell and molecular biology.

[32]  Jukon Kim,et al.  Root-Specific Expression of OsNAC10 Improves Drought Tolerance and Grain Yield in Rice under Field Drought Conditions1[W][OA] , 2010, Plant Physiology.

[33]  W. Yin,et al.  Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica , 2011, Journal of experimental botany.

[34]  Pil Joon Seo,et al.  Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. , 2010, The Plant journal : for cell and molecular biology.

[35]  A. Britt,et al.  Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage , 2009, Proceedings of the National Academy of Sciences.

[36]  K. Shinozaki,et al.  The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice , 2010, Molecular Genetics and Genomics.

[37]  Masakazu Satou,et al.  Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. , 2008, Plant & cell physiology.

[38]  Bernd Mueller-Roeber,et al.  A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. , 2010, The Plant journal : for cell and molecular biology.

[39]  C. Calkhoven,et al.  Multiple steps in the regulation of transcription-factor level and activity. , 1996, The Biochemical journal.

[40]  Li-li Huang,et al.  Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses , 2010, Molecular Biology Reports.

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

[42]  D. Llewellyn,et al.  ATAF NAC transcription factors: Regulators of plant stress signaling , 2010, Plant signaling & behavior.

[43]  J. Drenth,et al.  Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. , 2011, Molecular plant.

[44]  Rui An,et al.  A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis , 2006, Plant Molecular Biology.

[45]  Youn-sung Kim,et al.  Integration of Auxin and Salt Signals by the NAC Transcription Factor NTM2 during Seed Germination in Arabidopsis1[W] , 2011, Plant Physiology.

[46]  A. Gesteira,et al.  Analysis of the NAC transcription factor gene family in citrus reveals a novel member involved in multiple abiotic stress responses , 2011, Tree Genetics & Genomes.

[47]  Yongfeng Guo,et al.  AtNAP, a NAC family transcription factor, has an important role in leaf senescence. , 2006, The Plant journal : for cell and molecular biology.

[48]  L. Xiong,et al.  Systematic analysis of NPK1-like genes in rice reveals a stress-inducible gene cluster co-localized with a quantitative trait locus of drought resistance , 2008, Molecular Genetics and Genomics.

[49]  J. Randles,et al.  A NAC Domain Protein Interacts with Tomato leaf curl virus Replication Accessory Protein and Enhances Viral Replication , 2005, The Plant Cell Online.

[50]  Hui Peng,et al.  Characterization of a chickpea (Cicer arietinum L.) NAC family gene, CarNAC5, which is both developmentally- and stress-regulated. , 2009, Plant physiology and biochemistry : PPB.

[51]  Nobutaka Mitsuda,et al.  VOZ; isolation and characterization of novel vascular plant transcription factors with a one-zinc finger from Arabidopsis thaliana. , 2004, Plant & cell physiology.

[52]  R. Stolf-Moreira,et al.  Transcription factors expressed in soybean roots under drought stress. , 2011, Genetics and molecular research : GMR.

[53]  Marta de Torres-Zabala,et al.  Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. , 2008, The Plant journal : for cell and molecular biology.

[54]  Shoshi Kikuchi,et al.  Genome-wide analysis of NAC transcription factor family in rice. , 2010, Gene.

[55]  Faouzi Horchani,et al.  Prolonged root hypoxia effects on ethylene biosynthesis and perception in tomato fruit , 2011, Plant signaling & behavior.

[56]  K. Shinozaki,et al.  ABA-mediated transcriptional regulation in response to osmotic stress in plants , 2011, Journal of Plant Research.

[57]  Hui Peng,et al.  Cloning and Characterization of a Novel NAC Family Gene CarNAC1 from Chickpea (Cicer arietinum L.) , 2010, Molecular biotechnology.

[58]  Fengming Song,et al.  The Arabidopsis ATAF1, a NAC transcription factor, is a negative regulator of defense responses against necrotrophic fungal and bacterial pathogens. , 2009, Molecular plant-microbe interactions : MPMI.

[59]  S. Mukherjee,et al.  MicroRNA profiling of tomato leaf curl new delhi virus (tolcndv) infected tomato leaves indicates that deregulation of mir159/319 and mir172 might be linked with leaf curl disease , 2010, Virology Journal.

[60]  K. Shinozaki,et al.  Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[61]  D. Klessig,et al.  HRT-mediated hypersensitive response and resistance to Turnip crinkle virus in Arabidopsis does not require the function of TIP, the presumed guardee protein. , 2008, Molecular plant-microbe interactions : MPMI.

[62]  L. Xiong,et al.  Systematic Sequence Analysis and Identification of Tissue-specific or Stress-responsive Genes of Nac Transcription Factor Family in Rice , 2008 .

[63]  Xu Liu,et al.  Molecular Characterization of Arachis Hypogaea NAC 2 (AhNAC2) Reveals it as a NAC-Like Protein in Peanut , 2010 .

[64]  Xianming Chen,et al.  TaNAC8, a novel NAC transcription factor gene in wheat, responds to stripe rust pathogen infection and abiotic stresses , 2010 .

[65]  B. Han,et al.  Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. , 2009, Biochemical and biophysical research communications.

[66]  Kazuo Shinozaki,et al.  A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. , 2004, The Plant journal : for cell and molecular biology.

[67]  Tianzhen Zhang,et al.  Characterization of six novel NAC genes and their responses to abiotic stresses in Gossypium hirsutum L. , 2009 .

[68]  Qian Gao,et al.  Comprehensive Analysis of NAC Domain Transcription Factor Gene Family in Populus trichocarpa , 2010, BMC Plant Biology.

[69]  Junli Ye,et al.  Identification and Expression Pattern of a Novel NAM, ATAF, and CUC-Like Gene from Citrus sinensis Osbeck , 2009, Plant Molecular Biology Reporter.

[70]  J. Falk,et al.  Isolation of senescence‐related cDNAs from flag leaves of field grown barley plants , 2003 .

[71]  Hui Peng,et al.  A NAC transcription factor gene of Chickpea (Cicer arietinum), CarNAC3, is involved in drought stress response and various developmental processes. , 2009, Journal of plant physiology.

[72]  Chung-Mo Park,et al.  Membrane-bound transcription factors in plants. , 2008, Trends in plant science.

[73]  J. Culver,et al.  Interaction of the Tobacco Mosaic Virus Replicase Protein with a NAC Domain Transcription Factor Is Associated with the Suppression of Systemic Host Defenses , 2009, Journal of Virology.

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

[75]  M. K. Jensen,et al.  Senescence-associated Barley NAC (NAM, ATAF1,2, CUC) Transcription Factor Interacts with Radical-induced Cell Death 1 through a Disordered Regulatory Domain* , 2011, The Journal of Biological Chemistry.

[76]  R. Bahadur,et al.  Molecular Cloning and Characterization of a Membrane Associated NAC Family Gene, SiNAC from Foxtail Millet [Setaria italica (L.) P. Beauv.] , 2011, Molecular biotechnology.

[77]  Z. Ye,et al.  Molecular analysis of two salt-responsive NAC-family genes and their expression analysis in tomato , 2011, Molecular Biology Reports.

[78]  K. Shinozaki,et al.  Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. , 2006, Current opinion in plant biology.

[79]  Liang Zhao,et al.  Overexpression of a novel chrysanthemum NAC transcription factor gene enhances salt tolerance in tobacco , 2011, Biotechnology Letters.

[80]  Jie Chen,et al.  Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress , 2011, Planta.

[81]  Tetsuya Sakurai,et al.  LegumeTFDB: an integrative database of Glycine max, Lotus japonicus and Medicago truncatula transcription factors , 2010, Bioinform..

[82]  D. Choi,et al.  Expression of a novel NAC domain-containing transcription factor (CaNAC1) is preferentially associated with incompatible interactions between chili pepper and pathogens , 2005, Planta.

[83]  Youn-Sung Kim,et al.  Proteolytic processing of an Arabidopsis membrane-bound NAC transcription factor is triggered by cold-induced changes in membrane fluidity. , 2010, The Biochemical journal.

[84]  K. Mochida,et al.  Genome-wide analysis for identification of salt-responsive genes in common wheat , 2008, Functional & Integrative Genomics.

[85]  Xu Liu,et al.  Improved Drought and Salt Tolerance in Transgenic Arabidopsis Overexpressing a NAC Transcriptional Factor from Arachis hypogaea , 2011, Bioscience, biotechnology, and biochemistry.

[86]  S. Chen,et al.  AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. , 2005, The Plant journal : for cell and molecular biology.

[87]  N. Chua,et al.  SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals , 2002, Nature.

[88]  Pil Joon Seo,et al.  Genome-scale screening and molecular characterization of membrane-bound transcription factors in Arabidopsis and rice. , 2010, Genomics.

[89]  Jukon Kim,et al.  Rice NAC proteins act as homodimers and heterodimers , 2009, Plant Biotechnology Reports.

[90]  Daowen Wang,et al.  The Arabidopsis RING Finger E3 Ligase RHA2a Is a Novel Positive Regulator of Abscisic Acid Signaling during Seed Germination and Early Seedling Development1[C][W][OA] , 2009, Plant Physiology.

[91]  M. Deyholos,et al.  Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes , 2006, BMC Plant Biology.

[92]  S. Puranik,et al.  Electrophoretic mobility shift assay reveals a novel recognition sequence for Setaria italica NAC protein , 2011, Plant signaling & behavior.

[93]  K. Skriver,et al.  DNA-binding specificity and molecular functions of NAC transcription factors , 2005 .

[94]  R. Zhong,et al.  Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. , 2010, Molecular plant.

[95]  김상규.  (A) Membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination , 2009 .

[96]  C. Gutiérrez,et al.  GRAB proteins, novel members of the NAC domain family, isolated by their interaction with a geminivirus protein , 1999, Plant Molecular Biology.

[97]  L. Xiong,et al.  A structural view of the conserved domain of rice stress-responsive NAC1 , 2011, Protein & Cell.

[98]  Chung-Mo Park,et al.  The Arabidopsis NAC Transcription Factor VNI2 Integrates Abscisic Acid Signals into Leaf Senescence via the COR/RD Genes[W] , 2011, Plant Cell.

[99]  L. Xiong,et al.  Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice , 2008, Plant Molecular Biology.

[100]  Marta T. Bokowiec,et al.  Tobacco Transcription Factors: Novel Insights into Transcriptional Regulation in the Solanaceae1[C][W][OA] , 2008, Plant Physiology.

[101]  P. Holm,et al.  Characterization of barley (Hordeum vulgare L.) NAC transcription factors suggests conserved functions compared to both monocots and dicots , 2011, BMC Research Notes.

[102]  R. Kumar,et al.  Molecular characterization of stress-inducible GmNAC genes in soybean , 2009, Molecular Genetics and Genomics.

[103]  T. Kaneda,et al.  The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death , 2009, Plant signaling & behavior.

[104]  K. Shinozaki,et al.  Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. , 2003, The Plant journal : for cell and molecular biology.

[105]  M. Morgante,et al.  An analysis of sequence variability in eight genes putatively involved in drought response in sunflower (Helianthus annuus L.) , 2011, Theoretical and Applied Genetics.

[106]  D. Van Der Straeten,et al.  The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[107]  Kazuo Shinozaki,et al.  Isolation and Functional Analysis of Arabidopsis Stress-Inducible NAC Transcription Factors That Bind to a Drought-Responsive cis-Element in the early responsive to dehydration stress 1 Promoterw⃞ , 2004, The Plant Cell Online.

[108]  T. Higashi,et al.  Disruption of a novel gene for a NAC-domain protein in rice confers resistance to Rice dwarf virus. , 2009, The Plant journal : for cell and molecular biology.

[109]  Shoshi Kikuchi,et al.  Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. , 2003, DNA research : an international journal for rapid publication of reports on genes and genomes.

[110]  Kazuo Shinozaki,et al.  In silico Analysis of Transcription Factor Repertoire and Prediction of Stress Responsive Transcription Factors in Soybean , 2009, DNA research : an international journal for rapid publication of reports on genes and genomes.

[111]  T. Boller,et al.  Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding , 2001, Plant Molecular Biology.

[112]  G. Xue,et al.  TaNAC69 from the NAC superfamily of transcription factors is up-regulated by abiotic stresses in wheat and recognises two consensus DNA-binding sequences. , 2006, Functional plant biology : FPB.

[113]  Addie Nina Olsen,et al.  NAC transcription factors: structurally distinct, functionally diverse. , 2005, Trends in plant science.

[114]  K. Oda,et al.  Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis , 2009, Planta.

[115]  L. Xiong,et al.  Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice , 2006, Proceedings of the National Academy of Sciences.

[116]  M. K. Jensen,et al.  The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis , 2007, Plant Molecular Biology.

[117]  F. Nogueira,et al.  SsNAC23, a member of the NAC domain protein family, is associated with cold, herbivory and water stress in sugarcane , 2005 .

[118]  Birgit Kersten,et al.  PlnTFDB: updated content and new features of the plant transcription factor database , 2009, Nucleic Acids Res..

[119]  C. Lata,et al.  Role of DREBs in regulation of abiotic stress responses in plants. , 2011, Journal of experimental botany.

[120]  W. Deng,et al.  Molecular Cloning and Characterization of a NAC-like Gene in “Navel” Orange Fruit Response to Postharvest Stresses , 2007, Plant Molecular Biology Reporter.

[121]  K. Skriver,et al.  Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors , 2004, EMBO reports.