Journal of Plant Research

, Volume 129, Issue 5, pp 955–962 | Cite as

Arabidopsis ATAF1 enhances the tolerance to salt stress and ABA in transgenic rice

  • Yongchang Liu
  • Jie Sun
  • Yaorong Wu
Regular Paper


NAC (NAM, ATAF1/2, CUC2) transcription factors are plant-specific and have diverse functions in many plant developmental processes and responses to stress. In our previous study, we found that the expression of ATAF1, an Arabidopsis NAC gene, was obviously induced by high-salinity and abscisic acid (ABA). The overexpression of ATAF1 in Arabidopsis increased plant sensitivity to ABA and salt. To investigate whether ATAF1 affects the sensitivity of monocotyledon plant to salt and ABA, ATAF1 transgenic rice were generated. Transgenic rice exhibited significantly improved salt tolerance and insensitivity to ABA. The results of real-time PCR showed that ATAF1 overexpression in rice elevated the transcription of OsLEA3, OsSalT1 and OsPM1, which are stress-associated genes. Our results indicate that ATAF1 plays an important role in response to salt stress and may be utilized to improve the salt tolerance of rice.


ATAF1 NAC Rice Salt stress 

Supplementary material

10265_2016_833_MOESM1_ESM.docx (777 kb)
Supplementary material 1 (DOCX 776 kb)


  1. Aguan K, Sugawara K, Suzuki N, Kusano T (1991) Isolation of genes for low-temperature-induced proteins in rice by a simple subtractive method. Plant Cell Physiol 32:1285–1289Google Scholar
  2. Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C, Mehrnia M, Zanor MI, Kohler B, Mueller-Roeber B (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J 62:250–264CrossRefPubMedGoogle Scholar
  3. Brini F, Hanin M, Lumbreras V, Amara I, Khoudi H, Hassairi A, Pages M, Masmoudi K (2007) Overexpression of wheat dehydrin DHN-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana. Plant Cell Rep 26:2017–2026CrossRefPubMedGoogle Scholar
  4. Chen X, Wang Y, Lv B, Li J, Luo L, Lu S, Zhang X, Ma H, Ming F (2014) The NAC family transcription factor OsNAP confers abiotic stress response through the ABA pathway. Plant Cell Physiol 55:604–619CrossRefPubMedGoogle Scholar
  5. Chourey K, Ramani S, Apte SK (2003) Accumulation of LEA proteins in salt (NaCl) stressed young seedlings of rice (Oryza sativa L.) cultivar Bura Rata and their degradation during recovery from salinity stress. J Plant Physiol 160:1165–1174CrossRefPubMedGoogle Scholar
  6. Claes B, Dekeyser R, Villarroel R, Van den Bulcke M, Bauw G, Van Montagu M, Caplan A (1990) Characterization of a rice gene showing organ-specific expression in response to salt stress and drought. Plant Cell 2:19–27CrossRefPubMedPubMedCentralGoogle Scholar
  7. Ding Z, Yan J, Li C, Li G, Wu Y, Zheng S (2015) Transcription factor WRKY46 modulates the development of Arabidopsis lateral roots in osmotic/salt stress conditions via regulation of ABA signaling and auxin homeostasis. Plant J 84:56–69CrossRefPubMedGoogle Scholar
  8. Garapati P, Xue GP, Munne-Bosch S, Balazadeh S (2015) Transcription factor ATAF1 in Arabidopsis promotes senescence by direct regulation of key chloroplast maintenance and senescence transcriptional cascades. Plant Physiol 168:1122–1139CrossRefPubMedPubMedCentralGoogle Scholar
  9. He X, Mu R, Cao W, Zhang Z, Zhang J, Chen S (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916CrossRefPubMedGoogle Scholar
  10. Hong Y, Zhang H, Huang L, Li D, Song F (2016) Overexpression of a stress-responsive NAC tanscription factor gene ONAC022 improves drought and salt tolerance in rice. Front Plant Sci 7:4CrossRefPubMedPubMedCentralGoogle Scholar
  11. Hu H, Dai M, Yao J, 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 103:12987–12992CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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 67:169–181CrossRefPubMedGoogle Scholar
  13. Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145CrossRefPubMedPubMedCentralGoogle Scholar
  14. Huang X, Chao D, Gao J, Zhu M, Shi M, Lin H (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Gene Dev 23:1805–1817CrossRefPubMedPubMedCentralGoogle Scholar
  15. Jensen MK, Lindemose S, de Masi F, Reimer JJ, Nielsen M, Perera V, Workman CT, Turck F, Grant MR, Mundy J, Petersen M, Skriver K (2013) ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana. FEBS Open Bio 3:321–327CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291CrossRefPubMedGoogle Scholar
  17. Kim SG, Park CM (2007) Membrane-mediated salt stress signaling in flowering time control. Plant Signal Behav 2:517–518CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kim SG, Lee AK, Yoon HK, Park CM (2008) A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. Plant J 55:77–88CrossRefPubMedGoogle Scholar
  19. Kim IS, Kim YS, Yoon HS (2012) Rice ASR1 protein with reactive oxygen species scavenging and chaperone-like activities enhances acquired tolerance to abiotic stresses in Saccharomyces cerevisiae. Mol Cells 33:285–293CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kleinow THS, 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
  21. Koike M, Takezawa D, Arakawa K, Yoshida S (1997) Accumulation of 19-kDa plasma membrane polypeptide during induction of freezing tolerance in wheat suspension-cultured cells by abscisic acid. Plant Cell Physiol 38:707–716CrossRefPubMedGoogle Scholar
  22. Li Y, Feng D, Zhang D, Su J, Zhang Y, Li Z, Mu P, Liu B, Wang H, Wang J (2012) Rice MAPK phosphatase IBR5 negatively regulates drought stress tolerance in transgenic Nicotiana tabacum. Plant Sci 188–189:10–18CrossRefPubMedGoogle Scholar
  23. Lu P, Chen N, An R, Su Z, Qi B, Ren F, Chen J, Wang X (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 63:289–305CrossRefPubMedGoogle Scholar
  24. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158CrossRefPubMedGoogle Scholar
  25. 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 63:2933–2946CrossRefPubMedPubMedCentralGoogle Scholar
  26. Mao H, Wang H, Liu S, Li Z, Yang X, Yan J, Li J, Tran LS, Qin F (2015) A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun 6:8326CrossRefPubMedPubMedCentralGoogle Scholar
  27. Mauch-Mani B, Flors V (2009) The ATAF1 transcription factor: at the convergence point of ABA-dependent plant defense against biotic and abiotic stresses. Cell Res 19:1322–1323CrossRefPubMedGoogle Scholar
  28. 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 51:617–630CrossRefPubMedGoogle Scholar
  29. Ohnishi T, Sugahara S, Yamada T, Kikuchi K, Yoshiba Y, Hirano HY, Tsutsumi N (2005) OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genet Syst 80:135–139CrossRefPubMedGoogle Scholar
  30. Pospisilova H, Jiskrova E, Vojta P, Mrizova K, Kokas F, Cudejkova MM, Bergougnoux V, Plihal O, Klimesova J, Novak O, Dzurova L, Frebort I, Galuszka P (2016) Transgenic barley overexpressing a cytokinin dehydrogenase gene shows greater tolerance to drought stress. New Biotechnol. doi: 10.1016/j.nbt.2015.12.005 Google Scholar
  31. Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50:54–69CrossRefPubMedGoogle Scholar
  32. Qin F, Sakuma Y, Tran LS, Maruyama K, Kidokoro S, Fujita Y, Fujita M, Umezawa T, Sawano Y, Miyazono K, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20:1693–1707CrossRefPubMedPubMedCentralGoogle Scholar
  33. Sakuraba Y, Piao W, Lim JH, Han SH, Kim YS, An G, Paek NC (2015) Rice ONAC106 inhibits leaf senescence and increases salt tolerance and tiller angle. Plant Cell Physiol 56:2325–2339CrossRefPubMedGoogle Scholar
  34. Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 6:902CrossRefPubMedPubMedCentralGoogle Scholar
  35. Shekhawat UKS, Ganapathi TR (2014) Transgenic banana plants overexpressing MusabZIP53 display severe growth retardation with enhanced sucrose and polyphenol oxidase activity. Plant Cell Tissue Organ Culture 116:387–402CrossRefGoogle Scholar
  36. Song S, Chen Y, Chen J, Dai X, Zhang W (2011) Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. Planta 234:331–345CrossRefPubMedGoogle Scholar
  37. Souer E, Houwelingen A, Van Kloos D, Mol J, Koes R (1996) The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85:159–170CrossRefPubMedGoogle Scholar
  38. 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 284:173–183CrossRefPubMedGoogle Scholar
  39. Wang H, Hao J, Chen X, Hao Z, Wang X, Lou Y, Peng Y, Guo Z (2007) Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Mol Biol 65:799–815CrossRefPubMedGoogle Scholar
  40. Wang X, Basnayake BM, Zhang H, Li G, Li W, Virk N, Mengiste T, Song F (2009) The Arabidopsis ATAF1, a NAC transcription factor, is a negative regulator of defense responses against necrotrophic fungal and bacterial pathogens. Mol Plant Microbe Interact 22:1227–1238CrossRefPubMedGoogle Scholar
  41. Wang Y, Qu G, Li H, Wu Y, Wang C, Liu G, Yang C (2010) Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii. Mol Biol Rep 37:1119–1124CrossRefPubMedGoogle Scholar
  42. Wang T, Tohge T, Ivakov A, Mueller-Roeber B, Fernie AR, Mutwil M, Schippers JH, Persson S (2015) Salt-related MYB1 coordinates abscisic acid biosynthesis and signaling during salt stress in Arabidopsis. Plant Physiol 169:1027–1041CrossRefPubMedPubMedCentralGoogle Scholar
  43. Wu Y, Deng Z, Lai J, Zhang Y, Yang C, Yin B, Zhao Q, Zhang L, Li Y, Yang C, Xie Q (2009) Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res 19:1279–1290CrossRefPubMedGoogle Scholar
  44. Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Gene Dev 14:3024–3036CrossRefPubMedPubMedCentralGoogle Scholar
  45. Xu M, Li L, Fan Y, Wan J, Wang L (2011) ZmCBF3 overexpression improves tolerance to abiotic stress in transgenic rice (Oryza sativa) without yield penalty. Plant Cell Rep 30:1949–1957CrossRefPubMedGoogle Scholar
  46. Yang SD, Seo PJ, Yoon HK, Park CM (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23:2155–2168CrossRefPubMedPubMedCentralGoogle Scholar
  47. Yang A, Dai X, Zhang W (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:2541–2556CrossRefPubMedPubMedCentralGoogle Scholar
  48. Zhang W, Peumans WJ, Barre A, Astoul CH, Rovira P, Rouge P, Proost P, Truffa-Bachi P, Jalali AA, Van Damme EJ (2000) Isolation and characterization of a jacalin-related mannose-binding lectin from salt-stressed rice (Oryza sativa) plants. Planta 210:970–978CrossRefPubMedGoogle Scholar
  49. Zhang L, Li Y, Lu W, Meng F, Wu C, Guo X (2012) Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana. J Exp Bot 63:3935–3951CrossRefPubMedPubMedCentralGoogle Scholar
  50. Zhang D, Yang H, Li X, Li H, Wang Y (2014) Overexpression of Tamarix albiflonum TaMnSOD increases drought tolerance in transgenic cotton. Mol Breed 34:1–11CrossRefGoogle Scholar
  51. Zheng X, Chen B, Lu G, Han B (2009) Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophys Res Commun 379:985–989CrossRefPubMedGoogle Scholar
  52. Zhong R, Demura T, Ye Z (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170CrossRefPubMedPubMedCentralGoogle Scholar
  53. Zhu M, Chen G, Zhou S, Tu Y, Wang Y, Dong T, Hu Z (2014) A new tomato NAC (NAM/ATAF1/2/CUC2) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation. Plant Cell Physiol 55:119–135CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2016

Authors and Affiliations

  1. 1.State Key Laboratory of Plant Genomics, National Center for Plant Gene Research, Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingChina
  2. 2.College of Agriculture/The Key Laboratory of Oasis Eco-agricultureShihezi UniversityShiheziChina

Personalised recommendations