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An NAC transcription factor gene from Malus baccata, MbNAC29, increases cold and high salinity tolerance in Arabidopsis

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Abstract

NAC (no apical meristem [NAM], Arabidopsis thaliana transcription activation factor [ATAF1/2], and cup-shaped cotyledon [CUC2]) TFs are involved in stress responses in plants. However, their roles in abiotic stresses are still not well known in Malus plants. In the present study, MbNAC29 from Malus baccata was identified and characterized. Quantitative real-time PCR analysis revealed that the expression of MbNAC29 was induced by cold, high salinity, drought, and heat. The open reading frame (ORF) of MbNAC29 is 1122 bp, encodes 373 amino acids. Subcellular localization showed that the MbNAC29-GFP (green fluorescent protein) fusion protein was localized in the nucleus. Furthermore, MbNAC29 was highly expressed in new leaf and mature leaf. When MbNAC29 was introduced into Arabidopsis, it improved cold and high salinity tolerance in transgenic plants under low-temperature stress (− 4°C) and salt stress (200 mM NaCl). When MbNAC29 was introduced into Arabidopsis, it increased the survival rate of transgenic lines than wild type (WT) under cold and high-salinity stresses. In addition, overexpression of MbNAC29 in transgenic Arabidopsis increased the contents of chlorophyll and proline and the activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), while decreased the content of malondialdehyde (MDA). Therefore, these results suggest that MbNAC29 probably plays an important role in response to cold and salt stresses in Arabidopsis by enhancing scavenging capability of reactive oxygen species (ROS).

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References

  • 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 6:841–857

    Article  Google Scholar 

  • An G, Watson BD, Chiang CC (1986) Transformation of tobacco, tomato, potato, and Arabidopsis thaliana using a binary ti vector system. Plant Physiol 81:301–305

    Article  CAS  Google Scholar 

  • Christianson JA, Dennis ES, Llewellyn DJ, Wilson IW (2010) ATAF NAC TFs: regulators of plant stress signaling. Plant Signal Behav 5:428–432

    Article  CAS  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  Google Scholar 

  • Delaunay A, Pflieger D, Barrault MB (2002) A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111:471–481

    Article  CAS  Google Scholar 

  • Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431

    Article  CAS  Google Scholar 

  • Duval M, Hsieh TF, Kim SY, Thomas TL (2002) Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain super family. Plant Mol Biol 50:237–248

    Article  CAS  Google Scholar 

  • 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 Gen Genomics 280:547–563

    Article  CAS  Google Scholar 

  • Gong X, Liu J (2013) Genetic transformation and genes for resistance to abiotic and biotic stresses in citrus and its related genera. Plant Cell Tissue Organ Cult 113:137–147

    Article  CAS  Google Scholar 

  • Guo M, Liu J, Ma X, Luo D, Gong Z, Lu M (2016) The plant heat stress TFs (HSFs): structure, regulation, and function in response to abiotic stresses. Plant Sci 7:114–138

    Google Scholar 

  • Han D, Du M, Zhou Z, Wang S, Li T, Han J, Xu T, Yang G (2020a) Overexpression of a Malus baccata NAC transcription factor gene MbNAC25 increases cold and salinity tolerance in Arabidopsis. Int J Mol Sci 21:1198

    Article  CAS  Google Scholar 

  • Han D, Han J, Yang G, Wang S, Xu T, Yang G, Li W (2020b) An ERF transcription factor gene from Malus baccata (L.) Borkh, MbERF11, affects cold and salt stress tolerance in Arabidopsis. Forests 11:154

    Article  Google Scholar 

  • Han D, Hou Y, Ding H, Zhou Z, Li H, Yang G (2018a) Isolation and preliminary functional analysis of MbWRKY4 gene involved in salt tolerance in transgenic tobacco. Int J Agric Biol 20:2045–2052

    Google Scholar 

  • Han D, Wang Y, Zhang Z, Pu Q, Ding H, Han J, Fan T, Bai X, Yang G (2017) Isolation and functional analysis of MxCS3: a gene encoding a citrate synthase in Malus xiaojinensis, with functions in tolerance to iron stress and abnormal flower in transgenic Arabidopsis thaliana. Plant Growth Regul 82:479–489

    Article  CAS  Google Scholar 

  • Han D, Zhang Z, Ding H, Chai L, Liu W, Li H, Yang G (2018b) Isolation and characterization of MbWRKY2 gene involved in enhanced drought tolerance in transgenic tobacco. J Plant Interact 13:163–172

    Article  CAS  Google Scholar 

  • Han D, Zhang Z, Ding H, Wang Y, Liu W, Li H, Yang G (2018c) Molecular cloning and functional analysis of MbWRKY3 involved in improved drought tolerance in transformed tobacco. J Plant Interact 13:329–337

    Article  CAS  Google Scholar 

  • Han Y, Yang H, Wu M, Yi H (2019) Enhanced drought tolerance of foxtail millet seedlings by sulfur dioxide fumigation. Ecotoxicol Environ Saf 178:9–16

    Article  CAS  Google Scholar 

  • 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 44:903–916

    Article  CAS  Google Scholar 

  • Hegedus DYM, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53:383–397

    Article  CAS  Google Scholar 

  • Hickman R, Hill C, Penfold CA (2013) A local regulatory network around three NAC TFs in stress responses and senescence in Arabidopsis leaves. Plant J Cell Mol Biol 75:26–39

    Article  CAS  Google Scholar 

  • Hu H, Dai M, Yao J (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci U S A 103:12987–12992

    Article  CAS  Google Scholar 

  • Hu H, You J, Fang Y (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 72:169–181

    Article  CAS  Google Scholar 

  • Huang Q, Qian X, Jiang T, Zheng X (2019) Effect of eugenol fumigation treatment on chilling injury and CBF gene expression in eggplant fruit during cold storage. Food Chem 292:143–150

    Article  CAS  Google Scholar 

  • Jia F, Qi S, Li H, Liu P, Li P, Wu C (2014) Overexpression of late embryogenesis abundant 14 enhances Arabidopsis salt stress tolerance. Biochem Biophys Res Commun 454:505–511

    Article  CAS  Google Scholar 

  • Jiang Y, Lin L, Zhong S, Cai Y, Zhang F, Wang X, Miao R, Zhang B, Gao S, Hu X (2019) Overexpression of novel lncRNA NLIPMT inhibits metastasis by reducing phosphorylated glycogen synthase kinase 3 in breast cancer. J Cell Physiol 234:10689–10708

    Google Scholar 

  • Jin C, Li K, Xu X, Zhang H, Chen H, Chen Y (2017) A novel NAC transcription factor, PbeNAC1, of Pyrus betulifolia confers cold and drought tolerance via interacting with PbeDREBs and activating the expression of stress-responsive genes. Front Plant Sci 8:1049

    Article  Google Scholar 

  • Jin J, Zhang H, Kong L, Gao G, Luo G (2014) Plant TFDB 3.0: a portal for the functional and evolutionary study of plant TFs. Nucleic Acids Res 42:1182–1187

    Article  CAS  Google Scholar 

  • Li L, Lin G, Gu H, Yu L, Ni C (2019) Effects of Srxn1 on growth and Notch signaling of astrocyte induced by hydrogen peroxide. Artif Cells Nanomed Biotechnol 47:1917–1923

    Article  CAS  Google Scholar 

  • Liu Q, Xu K, Pan Y, Jiang B, Zhang H (2014) Functional analysis of a novel chrysanthemum WRKY transcription factor gene involved in salt tolerance. Plant Mol Biol Report 32:282–289

    Article  CAS  Google Scholar 

  • Liu S, Liu Y, Xu J, Liu T, Dong S (2019) Effectiveness of lysozyme coatings and 1-MCP treatments on storage and preservation of kiwifruit. Food Chem 288:201–217

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ma N, Zuo Y, Liang X, Yin B, Wang G (2013) The multiple stress-responsive transcription factor SlNAC1 improves the chilling tolerance of tomato. Physiol Plant 149:474–486

    Article  CAS  Google Scholar 

  • Mao H, Yu L, Han R, Li Z, Liu H (2016) ZmNAC55, a maize stress responsive NAC transcription factor, confers drought resistance in transgenic Arabidopsis. Plant Physiol Biochem 105:55–66

    Article  CAS  Google Scholar 

  • 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 63:2933–2946

    CAS  Google Scholar 

  • Meng C, Cai C, Zhang T, Guo W (2009) Characterization of six novel NAC genes and their responses to abiotic stresses in Gossypium hirsutum L. Plant Sci 176:352–359

    Article  CAS  Google Scholar 

  • Nakashima K, Tran LS, VanNguyen D, Fujita M, Maruyama K, Todaka D (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630

    Article  CAS  Google Scholar 

  • Nguyen KH, Mostofa MG, Li W, Ha CV, Watanabe Y, Le DT (2018) The soybean transcription factor GmNAC085 enhances drought tolerance in Arabidopsis. Environ Exp Bot 151:12–20

    Article  CAS  Google Scholar 

  • Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247

    Article  CAS  Google Scholar 

  • Puranik S, Sahu PP, Mandal SN (2013) Comprehensive genome-wide survey, genomic constitution and expression profiling of the NAC transcription factor family in foxtail millet (Setaria italica L.). PLoS One 8:564–594

    Article  CAS  Google Scholar 

  • Shahripour RB, Harrigan MR, Alexandrov AV (2014) N-acetylcysteine (NAC) in neurological disorders: mechanisms of action and therapeutic opportunities. Brain Behavior 4:108–122

    Article  Google Scholar 

  • Sharma A, Yuan HW, Kumar V, Ramakrishnan M, Kohli SK, Kaur R, Thukral AK, Bhardwaj R, Zheng BS (2019) Castasterone attenuates insecticide induced phytotoxicity in mustard. Ecotoxicol Environ Saf 179:50–61

    Article  CAS  Google Scholar 

  • Singh K, Foley RC, Onatesanchez L (2002) TFs in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  CAS  Google Scholar 

  • Sun W, Shen Y, Han M, Cao Y, Zhang Z (2014) An adaptive transposable element insertion in the regulatory region of the EO gene in the domesticated silkworm. Bombyx mori Mol Biol Evol 31:3302–3313

  • Tak H, Negi S, Ganapathi TR (2017) Banana NAC transcription factor Musa NAC042 is positively associated with drought and salinity tolerance. Protoplasman 254:803–816

    Article  CAS  Google Scholar 

  • Tang Y, Liu M, Gao S, Zhang Z, Zhao X, Zhao C (2012) Molecular of novel TaNAC genes in wheat and overexpression of TaNAC2a confers drought tolerance in tobacco. Physiol Plant 144:210–224

    Article  CAS  Google Scholar 

  • Tokihiko N, Masatomo K, Yoshu Y (1999) Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett 461:205–210

    Article  Google Scholar 

  • Tran LS, Quach TN, Guttikonda SK, Aldrich DL, Kumar R, Neelakandan A (2009) Molecular characterization of stress-inducible GmNAC genes in soybean. Mol Gen Genomics 281:647–664

    Article  CAS  Google Scholar 

  • Xiao H, Yin L, Xu X, Li T, Han Z (2008) The iron regulated transporter, MbNRAMP1, isolated from Malus baccata is involved in Fe, Mn and Cd trafficking. Ann Bot 102:881–889

    Article  CAS  Google Scholar 

  • Xie C, Zhang J, Zhou H, Li J, Zhang Z, Wang D, Chen S (2003) Serine/threonine kinase activity in the putative histidine kinase-like ethylene receptor NTHK1 from tobacco. Plant J 33:385–393

    Article  CAS  Google Scholar 

  • Yang G, Li J, Liu W, Yu Z, Shi Y, Lv B, Wang B, Han D (2015a) Molecular cloning and characterization of MxNAS2, a gene encoding nicotianamine synthase in Malus xiaojinensis, with functions intolerance to iron stress and misshapen flower in transgenic tobacco. Sci Hortic 183:77–86

    Article  CAS  Google Scholar 

  • Yang X, Wang X, Ji L, Yi Z, Fu C, Ran J, Hu R, Zhou G (2015b) Overexpression of a Miscanthus lutarioriparius NAC gene MlNAC5 confers enhanced drought and cold tolerance in Arabidopsis. Plant Cell Rep 34:943–958

    Article  CAS  Google Scholar 

  • Yang Y, Liu B, Xu J, Wang J, Wu J, Shi C (2017) Derivation of pluripotent stem cells with in vivo embryonic and extra embryonic potency. Cell 169:243–257

    Article  CAS  Google Scholar 

  • Yu X, Liu Y, Wang S, Tao Y, Wang Z, Shu Y, Peng H, Mijiti A, Wang Z, Zhang H (2015) CarNAC4, a NAC-type chickpea transcription factor conferring enhanced drought and salt stress tolerances in Arabidopsis. Plant Cell Rep 35:1–15

    Google Scholar 

  • Zhang X, Cheng Z, Zhao K (2019) Functional characterization of poplar NAC13 gene in salt tolerance. Plant Sci 281:1–8

    Article  CAS  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 379:985–989

    Article  CAS  Google Scholar 

  • Zuo W, Chao Q, Zhang N, Ye J, Tan G, Li B, Xing Y, Zhang B, Liu H, Fengler K (2015) A maize wall-associated kinase confers quantitative resistance to head smut. Nat Genet 47:151–157

    Article  CAS  Google Scholar 

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Funding

This project was supported by the National Natural Science Foundation of China (31301757), the Natural Science Fund Joint Guidance Project of Heilongjiang Province (LH2019C031), Young Talent Project of Northeast Agricultural University (19QC06), the Open Project of Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs (neauhc201803), Postdoctoral Scientific Research Development Fund of Heilongjiang Province, China (LBH-Q16020), and Fruit Tree Collaborative Innovation and Promotion System of Heilongjiang Province.

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Authors and Affiliations

  1. The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, College of Horticulture & Landscape Architecture, Northeast Agricultural University, Harbin, 150030, China

    Deguo Han, Man Du, Zhengyi Zhou, Shuang Wang, Tiemei Li, Jiaxin Han, Tianlong Xu & Guohui Yang

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  1. Deguo Han
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  2. Man Du
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  3. Zhengyi Zhou
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  4. Shuang Wang
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  6. Jiaxin Han
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  7. Tianlong Xu
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Correspondence to Tiemei Li or Guohui Yang.

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Editor: Yong Eui Choi

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Han, D., Du, M., Zhou, Z. et al. An NAC transcription factor gene from Malus baccata, MbNAC29, increases cold and high salinity tolerance in Arabidopsis. In Vitro Cell.Dev.Biol.-Plant 56, 588–599 (2020). https://doi.org/10.1007/s11627-020-10105-9

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