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Acta Physiologiae Plantarum

, Volume 35, Issue 5, pp 1397–1408 | Cite as

NAC (NAM/ATAF/CUC) transcription factors in different stresses and their signaling pathway

  • Zhuoyu Wang
  • Fenny Dane
Review

Abstract

Plants have evolved several molecular mechanisms to cope with biotic and abiotic stresses. Successful adaptation to stress is regulated through the activation or repression of the effects of transcription factors on specific target genes. The NAC (NAM, ATAF and CUC) transcription factors (TFs), which constitute one of the largest plant-specific transcription factor family, have been reported to be involved in plant development, biotic and abiotic stress regulation. Thus NAC TFs might be promising candidates for improving plants’ stress tolerance. Ongoing research on this transcription factor family has greatly broadened our knowledge in terms of its structure, functions, interaction with phytohormones, evolution and usage. This review focuses on the current status of NACs as regulators of stress.

Keywords

NAC Transcription factors Stresses Phytohormone 

References

  1. Anderson CL, Bremer K, Friis EM (2005) Dating phylogenetically basal eudicots using rbcL sequences and multiple fossil reference points. Am J Bot 92:1737–1748PubMedCrossRefGoogle Scholar
  2. Anjum SA, Xie XY, Wang LC, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. African Agric Research 6:2026–2032Google Scholar
  3. Avanci NC, Luche DD, Goldman GH, Goldman MHS (2010) Jasmonates are phytohormones with multiple functions, including plant defense and reproduction. Genet Mol Res 9:484–505PubMedCrossRefGoogle Scholar
  4. Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C, Mehrnia M, Zanor MI, Köhler B, Mueller-Roeber B (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J 62:250–264PubMedCrossRefGoogle Scholar
  5. Bollhoner B, Prestele J, Tuominen H (2012) Xylem cell death: emerging understanding of regulation and functions. J Exp Bot 63:1081–1094PubMedCrossRefGoogle Scholar
  6. Bostock RM (2005) Signal crosstalk and induced resistance: stradding the line between cost and benefit. Annu Rev Phytopathol 43:545–580PubMedCrossRefGoogle Scholar
  7. Boter M, Ruiz-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18:1577–1591PubMedCrossRefGoogle Scholar
  8. Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, Zhang CJ, Morris K, Jenner C, Jackson S, Thomas B, Tabrett A, Legaie R, Moore JD, Wild DL, Ott S, Rand D, Beynon J, Denby K, Mead A, Buchanan-Wollaston V (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23:873–894PubMedCrossRefGoogle Scholar
  9. Bu QY, Jiang HL, Li CB, Zhai QZ, Zhang JY, Wu XQ, Sun JQ, Xie Q, Li CY (2008) Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defence responses. Cell Res 18:756–767PubMedCrossRefGoogle Scholar
  10. Buchanan-Wollaston, Page T, Harrison E, Breeze E, Lim PO, Nam GH, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585PubMedCrossRefGoogle Scholar
  11. Carviel JL, Al-Daoud F, Neumann M, Mohammad A, Provart NJ, Moeder W, Yoshioka K, Cameron RK (2009) Forward and reverse genetics to identify genes involved in the age-related resistance response in Arabidopsis thaliana. Mol Plant Pathol 10:621–634PubMedCrossRefGoogle Scholar
  12. Chen Q, Wang Q, Xiong L, Lou Z (2011) A structural view of the conserved domain of rice stress-responsive NAC1. Protein Cell 2:55–63PubMedCrossRefGoogle Scholar
  13. Davies TJ, Barraclough TG, Chase MW, Soltis PS, Soltis DE, Savolainen V (2004) Darwin’s abominable mystery: insights from a supertree of the angiosperms. Proc Natl Acad Sci USA 101:1904–1909PubMedCrossRefGoogle Scholar
  14. Delessert C, Kazan K, Wilson IW, Van Der Straeten D, Manners J, Dennis ES, Dolferus R (2005) The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant J 43:745–757PubMedCrossRefGoogle Scholar
  15. Devoto A, Nieto-Rostro M, Xie D, Ellis C, Harmston R, Patrick E, Davis J, Sherratt L, Coleman M, Turner JG (2002) COI1 links jasmonate signaling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J 32:457–466PubMedCrossRefGoogle Scholar
  16. Duval M, Hsieh TF, Kim SY, Thomas TL (2002) Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Mol Biol 50:237–248PubMedCrossRefGoogle Scholar
  17. Ernst HA, Olsen AN, Skriver K, Larsen S, Leggio LL (2004) Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep 5:297–303PubMedCrossRefGoogle Scholar
  18. Fang Y, You J, Xie K, Xie W, Xiong L (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics 280:547–563PubMedCrossRefGoogle Scholar
  19. Faria JAQA, Reis PAB, Reis MTB, Rosado GL, Pinheiro GL, Mendes GC, Fontes EPB (2011) The NAC domain-containing protein, GmNAC6, is a downstream component of the ER stress- and osmotic stress-induced NRP-mediated cell-death signaling pathway. BMC Plant Biol 11:129PubMedCrossRefGoogle Scholar
  20. Finkler A, Ashery-Padan R, Fromm H (2007) CAMTAs: calmodulin-binding transcription activators from plants to human. FEBS Lett 581:3893–3898PubMedCrossRefGoogle Scholar
  21. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki KA (2004) Dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876PubMedCrossRefGoogle Scholar
  22. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view fromthe points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442PubMedCrossRefGoogle Scholar
  23. Galon Y, Finkler A, Fromm H (2010) Calcium-regulated transcription in plants. Molecular Plant 3:653–669PubMedCrossRefGoogle Scholar
  24. Gepstein S, Dabehi G, Carp MJ, Hajouj T, Nesher MFO, Yariv I, Dor C, Brassani M (2003) Large-scale identification of leaf senescence-associated genes. Plant J 36:629–642PubMedCrossRefGoogle Scholar
  25. Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2002) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12:1117–1126Google Scholar
  26. Gibson SI (2004) Sugar and phytohormone response pathways: navigating a signaling network. J Exp Botany 55:253–264CrossRefGoogle Scholar
  27. Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612PubMedCrossRefGoogle Scholar
  28. Halliwell B (2006) Reactive species and antioxidants: redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322PubMedCrossRefGoogle Scholar
  29. Hao YJ, Song QX, Chen HW, Zou HF, Wei W, Kang XS, Ma B, Zhang WK, Zhang JS, Chen SY (2010) Plant NAC-type transcription factor proteins contain a NARD domain for repression of transcriptional activation. Planta 232:1033–1043PubMedCrossRefGoogle Scholar
  30. Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, Zou HF, Lei G, Tian AG, Zhang WK, Ma B, Zhang JS, Chen SY (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68:302–313PubMedCrossRefGoogle Scholar
  31. He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916PubMedCrossRefGoogle Scholar
  32. Hu H, Dai M, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992PubMedCrossRefGoogle Scholar
  33. Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181PubMedCrossRefGoogle Scholar
  34. Hu R, Qi G, Kong YZ, Kong DJ, Gao Q, Zhou GK (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145PubMedCrossRefGoogle Scholar
  35. Hui S, Yanbin Y, Fang C, Ying X, Richard AD (2009) A bioinformatic analysis of NAC genes for plant cell wall development in relation to lignocellulosic bioenergy production. Bioenerg Res 2:217–232CrossRefGoogle Scholar
  36. Iba K (2002) Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu Rev Plant Biol 53:225–245PubMedCrossRefGoogle Scholar
  37. Jaillon O, Aury JM, Noel B, Policriti A, Crepet C et al (2007) The grapevine genome sequence suggests ancestral hexaplodization in major angiosperm phyla. Nature 449:463–467PubMedCrossRefGoogle Scholar
  38. Jensen MJ, Jesper JH, Gregersen PL, Gjetting T, Fuglsang AT, Hansen M, Joehnk N, Lyngkjaer MF, Collinge DB (2007) The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis. Plant Mol Biol 65:137–150PubMedCrossRefGoogle Scholar
  39. Jensen MK, Kjaersgaard T, Nielsen ML, Galberg P, Petersen K, O’Shea C, Skriver K (2010) The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANA019 stress signaling. Biochem J 426:183–196PubMedCrossRefGoogle Scholar
  40. Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Choi YD, Kim M, Reuzeau C, Kim JK (2012) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:186–197Google Scholar
  41. Kaneda T, Taga Y, Takai R, Iwano M, Matsui H, Takayama S, Isogai A, Che FS (2009) The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. EMBO J 28:926–936PubMedCrossRefGoogle Scholar
  42. Kato H, Motomura T, Komeda Y, Saito T, Kato A (2010) Overexpression of the NAC transcription factor family gene ANAC036 results in a dwarf phenotype in Arabidopsis thaliana. J Plant Physiol 167:571–577PubMedCrossRefGoogle Scholar
  43. Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park C-M (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18:3132–3144PubMedCrossRefGoogle Scholar
  44. Kim SG, Kim SY, Park CM (2007a) A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226:647–654PubMedCrossRefGoogle Scholar
  45. Kim SY, Kim SG, Kim YS, Seo PJ, Bae M, Yoon HK, Park CM (2007b) Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation. Nucleic Acids Res 35:203–213PubMedCrossRefGoogle Scholar
  46. Kim HS, Park BO, Yoo JH, Jung MS, Lee SM, Han HJ, Kim KE, Kim SH, Lim CO, Yun DJ, Lee SY, Chung WS (2007c) Identification of a calmodulin-binding NAC protein as a transcriptional repressor in Arabidopsis. J Biol Chem 282:36292–36302PubMedCrossRefGoogle Scholar
  47. Kimura M, Yamamoto YY, Seki M, Sakarai T, Sato M, Abe T, Yoshida S, Manabe K, Shinozaki K, Matsui M (2003) Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem Photobiol 77:226–233PubMedGoogle Scholar
  48. Kjaersgaard T, Jensen MK, Christiansen MW, Gregersen P, Kragelund BB, Skriver K (2011) Senescence-associated barley NAC (NAM, ATAF1,2, CUC) transcription factor interacts with radical-induced cell death 1 through a disordered regulatory domain. J Biol Chem 286:35418–35429PubMedCrossRefGoogle Scholar
  49. Kleinow T, Himbert S, Krenz B, Jeske H, Koncz C (2009) NAC domain transcription factor ATAF1 interacts with SNF1-related kinases and silencing of its subfamily causes severe developmental defects in Arabidopsis. Plant Sci 177:360–370CrossRefGoogle Scholar
  50. Li DT, Nishiyama R, Watanabe Y, Michida K, Yamaguchi-Shinizaki K, Shinozaki K, Tran LSP (2011a) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18:263–276CrossRefGoogle Scholar
  51. Li P, Wind JJ, Shia XL, Zhang HL, Hanson J, Smeekens SC, Teng S (2011b) Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane bound domain. Proc Natl Acad Sci USA 108:3436–3441PubMedCrossRefGoogle Scholar
  52. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136PubMedCrossRefGoogle Scholar
  53. Lin JF, Wu SH (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39:612–628PubMedCrossRefGoogle Scholar
  54. Lin RM, Zhao WS, Meng XB, Wang M, Peng YL (2007) Rice gene OsNAC19 encodes a novel NAC-domain transcription factor and responds to infection by Magnaporthe grisea. Plant Sci 172:120–130CrossRefGoogle Scholar
  55. Liu YZ, Baig MNR, Fan R, Ye JL, Cao YC, Deng XX (2009) Identification and expression pattern of a novel NAM, ATAF, and CUC-Like gene from Citrus sinensis Osbeck. Plant Mol Biol Rep 27:292–297CrossRefGoogle Scholar
  56. Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) JASMONATE-INSENSITIVE 1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950PubMedCrossRefGoogle Scholar
  57. Lu PL, Chen NZ, An R, Su Z, Qi BS, Ren F, Chen J, Wang XC (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 63:289–305PubMedCrossRefGoogle Scholar
  58. Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 10:1–14Google Scholar
  59. Maor R, Shirasu K (2005) The arms race continues: battle strategies between plants and fungal pathogens. Curr Opin Microbiol 8:399–404PubMedCrossRefGoogle Scholar
  60. Matts J, Jagadeeswaran G, Roe B-A, Sunkar R (2010) Identification of microRNAs and their targets in switchgrass, a model biofuel plant species. J Plant Physiol 167:896–904PubMedCrossRefGoogle Scholar
  61. Meuwly P, Mölders W, Buchala A, Métraux JP (1995) Local and systemic biosynthesis of salicylic acid in infected cucumber plants. Plant Physiol 109:1107–1114Google Scholar
  62. Morishita T, Kojima Y, Maruta T, Nishizawa-Yokoi A, Yabuta Y, Shigeoka S (2009) Arabidopsis NAC transcription factor, ANAC078, regulates flavonoid biosynthesis under high-light. Plant Cell Physiol 50:2210–2222PubMedCrossRefGoogle Scholar
  63. Muller CW (2001) Transcription factors: global and detailed views. Curr Opin Struct Biol 11:26–32PubMedCrossRefGoogle Scholar
  64. Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630PubMedCrossRefGoogle Scholar
  65. Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Schinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103Google Scholar
  66. Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, OOka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44PubMedCrossRefGoogle Scholar
  67. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87PubMedCrossRefGoogle Scholar
  68. Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive Analysis of NAC Family Genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247PubMedCrossRefGoogle Scholar
  69. Overmyer K, Brosche M, Kangasjarvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342PubMedCrossRefGoogle Scholar
  70. Overmyer K, Brosché M, Pellinen R, Kuittinen T, Tuominen H, Ahlfors R, Keinänen M, Saarma M, Scheel D, Kangasjärvi J (2005) Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death 1 mutant. Plant Physiol 137:1092–1104PubMedCrossRefGoogle Scholar
  71. Park J, Kim YS, Kim SG, Jung JH, Woo JC, Park CM (2011) Integration of auxin and salt signals by the NAC transcription factor NTM2 during seed germination in Arabidopsis. Plant Physiol 156:537–549PubMedCrossRefGoogle Scholar
  72. Peng H, Cheng HY, Chen C, Yu XW, Yang JN, Gao WR, Shi QH, Zhang H, Li JG, Ma H (2009a) A NAC transcription factor gene of chickpea (Cicer arietinum), CarNAC3, is involved in drought stress responses and various developmental processes. J Plant Physiol 166:1934–1945PubMedCrossRefGoogle Scholar
  73. Peng H, Cheng HY, Yu XW, Shi QH, Zhang H, Li JG, Ma H (2009b) Characterization of a chickpea (Cicer arietinum L.) NAC family gene, CarNAC5, which is both developmentally- and stress-regulated. Plant Physiol Biochem 47:1037–1045PubMedCrossRefGoogle Scholar
  74. Pinheiro GL, Marques CS, Costa MDBI, Reis PAB, Alves MS, Carvalho CM, Fietto LG, Fontes EPB (2009) Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444:10–23PubMedCrossRefGoogle Scholar
  75. Popescu SC, Popescu GV, Bachan S, Zhang Z, Seay M, Gerstein M, Snyder M, Dinesh-Kumar SP (2007) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc Natl Acad Sci U S A 104:4730–4735PubMedCrossRefGoogle Scholar
  76. Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381PubMedCrossRefGoogle Scholar
  77. Raskin (1992) Role of salicylic acid in plants. Annu Rev Plant Physiol Plant Mol Bioi 43:439–463Google Scholar
  78. Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–719PubMedGoogle Scholar
  79. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696PubMedCrossRefGoogle Scholar
  80. Rosahl S, Feussner I (2005) Oxylipins. In: Murphy DJ (ed) Plant lipids: biology. utilization and manipulation. Blackwell publishing Ltd/CRC press, Oxford and Boca Raton, pp 329–354Google Scholar
  81. Rushton PJ, Bokowiec MT, Han S, Zhang H, Brannock JF, Chen X, Laudeman TW, Timko MP (2008) Tobacco transcription factors: novel insights into transcriptional regulation in the Solanaceae. Plant Physiol 147:280–295PubMedCrossRefGoogle Scholar
  82. Safrany J, Haasz V, Mate Z, Ciolfi A, Feher B, Oravecz A, Stec A, Dallmann G, Morelli G, Ulm R, Nagy F (2008) Identification of a novel cis-regulatory element for UV-B-induced transcription in Arabidopsis. Plant J 54:402–414PubMedCrossRefGoogle Scholar
  83. Seo PJ, Kim SG, Park C-M (2008) Membrane-bound transcription factors in plants. Trends Plant Sci 13:550–556PubMedCrossRefGoogle Scholar
  84. Shen H, Yin Y-B, Chen FXY, Dixon RA (2009) A bioinformatic analysis of NAC genes for plant cell wall development in relation to lignocellulosic bioenergy production. Bioenerg Res 2:217–232CrossRefGoogle Scholar
  85. Si Y, Zhang C, Meng S, Dane F (2009) Gene expression changes in response to drought stress in Citrullus colocynthis. Plant Cell Rep 28:997–1009PubMedCrossRefGoogle Scholar
  86. Simillion C, Van de Poele K, Van Montagu MC, Zabeau M, Van de Peer Y (2002) The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 99:13627–13632PubMedCrossRefGoogle Scholar
  87. Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu J-K, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709PubMedCrossRefGoogle Scholar
  88. Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics 284:173–183PubMedCrossRefGoogle Scholar
  89. Tamaoki M, Freeman JL, Marqusè L, Pilon-Smits EAH (2008) New insights into the roles of ethylene and jasmonic acid in the acquisition of selenium resistance in plants. Plant Signal Behav 3:865–867Google Scholar
  90. Tang H, Bowers JE, Wang X, Patersona AH (2009) Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc Natl Acad Sci USA 107:472–477PubMedCrossRefGoogle Scholar
  91. Tran LSP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) 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 promoter. Plant Cell 16:2481–2498PubMedCrossRefGoogle Scholar
  92. Tran LSP, Nishiyama R, Yamaguchi-Shinozaki K, Shinozaki K (2009a) Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops 1:32–39CrossRefGoogle Scholar
  93. Tran LS, Quach TN, Guttikonda SK, Aldrich DL, Kumar R, Neelakandan A, Valliyodan B, Nguyen HT (2009b) Molecular characterization of stress-inducible GmNAC genes in soybean. Mol Genet Genomics 281:647–664PubMedCrossRefGoogle Scholar
  94. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604PubMedCrossRefGoogle Scholar
  95. Tuteja N, Sopory SK (2008) Chemical signaling under abiotic stress environment in plants. Plant Behavior 3:525–536CrossRefGoogle Scholar
  96. Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223CrossRefGoogle Scholar
  97. Walker EL, Connolly EL (2008) Time to pump iron: iron-deficiency-signaling mechanisms of higher plants. Current Opin Plant Biol 11:530–535CrossRefGoogle Scholar
  98. Welner DH, Lindemose S, Grossmann JG, Møllegaard, Olsen AN, Helgstrand C, Skriver K, Leggio LL (2012) DNA binging by the plant specific NAC transcription factors in crystal and solution: a firm link to WRKY and GCM transcription factors. Biochem Journal doi: 10.1042/BJ20111742
  99. Wu A, Allu AD, Garapati P, Siddiqui H, Dortay H, Zanor MI, Asensi-Fabado MA, Munne′ -Bosch S, Antonio C, Tohge T, Fernie AR, Kaufmann K, Xue GP, Mueller-Roeber B, Balazadeh S (2012) JUNGBRUNNEN1, a reactive oxygen species–responsive nac transcription factor, regulates longevity in Arabidopsis. Plant Cell 24:482–506PubMedCrossRefGoogle Scholar
  100. Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094PubMedCrossRefGoogle Scholar
  101. Xie Q, Frugis G, Colgan D, Chun NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036PubMedCrossRefGoogle Scholar
  102. Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant response to osmotic stress. Plant Cell Environ 25:131–139PubMedCrossRefGoogle Scholar
  103. Xu L, Liu F, Lechner E, Genschik P, Crosby WL, Ma H, Peng W, Huang D, Xi D (2002) The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14:1919–1935PubMedCrossRefGoogle Scholar
  104. Xu G, Ma H, Nei M, Kong H (2009) Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. Proc Natl Acad Sci USA 106:835–840PubMedCrossRefGoogle Scholar
  105. Yang SD, Yoon HK, Park CM (2011) The Arabidopsis NAC transciption factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23:2155–2168PubMedCrossRefGoogle Scholar
  106. Yoon HK, Kim SG, Kim SY, Park CM (2008) Regulation of leaf senescence by NTL-9 mediated osmotic stress signaling in Arabidopsis. Mol Cells 25:438–445PubMedGoogle Scholar
  107. Yoshida S (2003) Molecular regulation of leaf senescence. Curr Opin Plant Biol 6:79–84PubMedCrossRefGoogle Scholar
  108. Yoshii M, Yamazaki M, Rakawal R, Kishi-Kaboshi M, Miyao K, Hirochika H (2010) The NAC transcription factor RIM1 of rice is a new regulator of jasmonate signaling. Plant J 61:804–815PubMedCrossRefGoogle Scholar
  109. Zhu T, Nevo E, Sun D, Peng J (2012) Phylogenetic analyses unravel the evolutionary history of NAC proteins in plants. Evolution. doi: 10.1111/j.1558-5646.2011.01553.x PubMedGoogle Scholar
  110. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) Genevestigator Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632PubMedCrossRefGoogle Scholar
  111. Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot 61:1959–1968PubMedCrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2013

Authors and Affiliations

  1. 1.Department of HorticultureAuburn UniversityAuburnUSA

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