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A novel NAC transcription factor from Suaeda liaotungensis K. enhanced transgenic Arabidopsis drought, salt, and cold stress tolerance

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Abstract

Key message

Sl NAC1 functions as a stress-responsive NAC protein involved in the abscisic acid-dependent signaling pathway and enhances transgenic Arabidopsis drought, salt, and cold stress tolerance.

Abstract

NAC (NAM, ATAF1, 2, CUC2) transcription factors constitute the largest families of plant-specific transcription factors, known to be involved in various growth or developmental processes and in regulation of response to environmental stresses. However, only little information regarding stress-related NAC genes is available in Suaeda liaotungensis K. In this study, we cloned a full-length NAC gene (1,011 bp) named SlNAC1 using polymerase chain reaction from Suaeda liaotungensis K. and investigated its function by overexpression in transgenic Arabidopsis. SlNAC1 contains an NAC-conserved domain. Its expression in S. liaotungensis was induced by drought, high-salt, and cold (4 °C) stresses and by abscisic acid. Subcellular localization experiments in onion epidermal cells indicated that SlNAC1 is localized in the nucleus. Yeast one-hybrid assays showed that SlNAC1 functions as a transcriptional activator. SlNAC1 transgenic Arabidopsis displayed a higher survival ratio and lower rate of water loss under drought stress; a higher germination ratio, higher survival ratio, and lower root inhibition rate under salt stress; a higher survival ratio under cold stress; and a lower germination ratio and root inhibition rate under abscisic acid treatment, compared with wild-type Arabidopsis. These results suggested that SlNAC1 functions as a stress-responsive NAC protein involved in the abscisic acid-dependent signaling pathway and may have potential applications in transgenic breeding to enhance crops’ abiotic stress tolerances.

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Abbreviations

ABA:

Abscisic acid

CBF:

Core binding factor

DREB:

Dehydration response element binding factor

GFP:

Green fluorescent protein

MYB:

Myeloblastosis

NAC:

NAM (no apical meristem), ATAF1 or ATAF2 and CUC2 (cup-shaped cotyledon)

ORF:

Open reading frame

PEG 6000:

Polyethylene glycol 6000

RT-qPCR:

Real-time quantitative polymerase chain reaction

SNAC :

Stress-responsive NAC

TFs:

Transcription factors

References

  • Agarwal P, Jha B (2010) Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol Plant 54:201–212

    Article  CAS  Google Scholar 

  • Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    Article  CAS  PubMed  Google Scholar 

  • Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Dracup M, Turner N, Tang C, Reader M, Palta J, Gladstones J, Atkins C, Hamblin J (1998) Responses to abiotic stresses. Lupins as crop plants: biology, production and utilization. Wallingford, UK, 1998, pp 227–262

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran L-SP, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

    Article  CAS  PubMed  Google Scholar 

  • 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 68:302–313

    Article  CAS  PubMed  Google Scholar 

  • 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. PNAS USA 103:12987–12992

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O’Shea C, Skriver K (2009) The Arabidopsis thaliana NAC transcription factor family: structure–function relationships and determinants of ANAC019 stress signalling. Biochem J 426:183–196

    Article  Google Scholar 

  • Kim MJ, Park MJ, Seo PJ, Song JS, Kim HJ, Park CM (2012) Controlled nuclear import of the transcription factor NTL6 reveals a cytoplasmic role of SnRK2.8 in the drought-stress response. Biochem J 448:353–363

    Article  CAS  PubMed  Google Scholar 

  • Li C, Lv J, Zhao X, Ai X, Zhu X, Wang M, Zhao S, Xia G (2010) TaCHP: a wheat zinc finger protein gene down-regulated by abscisic acid and salinity stress plays a positive role in stress tolerance. Plant Physiol 154:211–221

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu G, Li X, Jin S, Liu X, Zhu L, Nie Y, Zhang X (2014) Overexpression of Rice NAC Gene SNAC1 improves drought and salt tolerance by enhancing root development and reducing transpiration rate in transgenic cotton. PLoS One 9:e86895

    Article  PubMed Central  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta CT) Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu M, Ying S, Zhang DF, Shi YS, Song YC, Wang TY, Li Y (2012) A maize stress-responsive NAC transcription factor, ZmSNAC1, confers enhanced tolerance to dehydration in transgenic Arabidopsis. Plant Cell Rep 31:1701–1711

    Article  CAS  PubMed  Google Scholar 

  • Mao X, Chen S, Li A, Zhai C, Jing R (2014) Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances in Arabidopsis. PLoS ONE 9:e84359

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 19:1322–1323

    Article  CAS  PubMed  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101:6309–6314

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2011) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103

    Article  CAS  PubMed  Google Scholar 

  • Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381

    Article  CAS  PubMed  Google Scholar 

  • Ren T, Qu F, Morris TJ (2000) HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell 12:1917–1926

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr Opin Biotechnol 14:194–199

    Article  CAS  PubMed  Google Scholar 

  • Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61:661–671

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Souer E, van Houwelingen A, 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 85:159–170

    Article  CAS  PubMed  Google Scholar 

  • 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 284:173–183

    Article  CAS  PubMed  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  CAS  PubMed  Google Scholar 

  • Tran LS, 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 16:2481–2498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Udvardi MK, Kakar K, Wandrey M, Montanari O, Murray J, Andriankaja A, Zhang JY, Benedito V, Hofer JM, Chueng F, Town CD (2007) Legume transcription factors: global regulators of plant development and response to the environment. Plant Physiol 144:538–549

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vilela B, Moreno-Cortes A, Rabissi A, Leung J, Pages M, Lumbreras V (2013) The maize OST1 kinase homolog phosphorylates and regulates the maize SNAC1-type transcription factor. PLoS One 8:e58105

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu Y, Deng Z, Lai J, Zhang Y, Yang C, Yin B, Zhao Q, Zhang L, Li Y, Xie Q (2009) Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res 19:1279–1290

    Article  CAS  PubMed  Google Scholar 

  • Yanhui C, Xiaoyuan Y, Kun H, Meihua L, Jigang L, Zhaofeng G, Zhiqiang L, Yunfei Z, Xiaoxiao W, Xiaoming Q (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124

    Article  CAS  PubMed  Google Scholar 

  • 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 379:985–989

    Article  CAS  PubMed  Google Scholar 

  • Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Dr Shaoming Tong (Liaoning Normal University) for kindly providing the pEGAD vector and seeds of Arabidopsis thaliana and Dr Qiao Su (Dalian University of Technology) for providing the GeneGun (GJ-1000, China). This work was supported by grants from the National Natural Science Foundation of China (No. 31340052) and Liaoning Provincial Natural Science Foundation of China (2013020069).

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Authors and Affiliations

  1. College of Life Sciences, Liaoning Normal University; Key Laboratory of Plant Biotechnology in Liaoning Province, 1 South Liushu Street, Ganjingzi District, Dalian, 116081, Liaoning, China

    Xiao-lan Li, Xing Yang, Yu-xin Hu, Xiao-dong Yu & Qiu-li Li

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  1. Xiao-lan Li
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  2. Xing Yang
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  3. Yu-xin Hu
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  4. Xiao-dong Yu
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Correspondence to Qiu-li Li.

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Communicated by Q. Zhao.

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Li, Xl., Yang, X., Hu, Yx. et al. A novel NAC transcription factor from Suaeda liaotungensis K. enhanced transgenic Arabidopsis drought, salt, and cold stress tolerance. Plant Cell Rep 33, 767–778 (2014). https://doi.org/10.1007/s00299-014-1602-y

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