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Molecular Characterization of Six Tissue-Specific or Stress-Inducible Genes of NAC Transcription Factor Family in Tomato (Solanum lycopersicum)

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Abstract

NAC (NAM/ATAF1/2/CUC2) transcription factors comprise a large plant-specific gene family and play crucial roles in plant growth, development, and stress response. However, only little information regarding development- or stress-related NAC genes is available in tomato. In this study, six tomato NAC genes, designated as SlNAC5-SlNAC10, were characterized to encode NAC proteins that share high similarity with those known plant NACs, especially in the NAC domain. These SlNAC genes, except SlNAC10, have a conserved exon–intron structure despite their different intron length. Phylogenetic analysis suggested that SlNAC5, SlNAC7, and SlNAC10 may belong to the development-related NACs. Quantitative RT-PCR analysis revealed that the six SlNACs exhibited different tissue-specific (such as roots, leaves, and flowers) expression profiles, suggesting that they may have crucial and diverse roles during tomato growth and development. Varying degrees of induction were detected in the transcript level of these SlNACs except SlNAC6 when treated with multiple hormones including ABA, ACC, GA3, MeJA, and IAA. The expression of SlNAC5-SlNAC10 was also checked under various abiotic stresses including NaCl, wounding, dehydration, and high/low temperature; six SlNACs were induced by these stresses with differential/similar induction levels. SlNAC5 was the most induced gene by NaCl stress with a 950-fold induction. Collectively, the results in this study of tissue-specific and/or stress-responsive SlNAC genes provide valuable information for further exploring the functional roles of NAC genes during tomato development and in response to environmental stresses, and one or more of them may hold promise for improving stress tolerance in transgenic tomato.

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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 9(6):841–857

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Benedetti CE, Costa CL, Turcinelli SR, Arruda P (1998) Differential expression of a novel gene in response to coronatine, methyl jasmonate, and wounding in the coi1 mutant of Arabidopsis. Plant Physiol 116(3):1037–1042

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berger Y, Harpaz-Saad S, Brand A, Melnik H, Sirding N, Alvarez JP, Zinder M, Samach A, Eshed Y, Ori N (2009) The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136(5):823–832

    Article  CAS  PubMed  Google Scholar 

  • Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H, Hay A, Johansen IE, Tsiantis M, Laufs P (2008) A conserved molecular framework for compound leaf development. Science 322(5909):1835–1839

    Article  CAS  PubMed  Google Scholar 

  • Collinge M, Boller T (2001) Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol Biol 46(5):521–529

    Article  CAS  PubMed  Google Scholar 

  • Delessert C, Kazan K, Wilson IW, Straeten DVD, Manners J, Dennis ES, Dolferus R (2005) The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant J 43(5):745–757

    Article  CAS  PubMed  Google Scholar 

  • Expósito-Rodríguez M, Borges AA, Borges-Pérez A, Pérez JA (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol 8(1):131

    Article  PubMed Central  PubMed  Google Scholar 

  • Fang Y, You J, **e K, **e W, **ong 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(6):547–563

    Article  CAS  PubMed  Google Scholar 

  • 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(6):863–876

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46(4):601–612

    Article  CAS  PubMed  Google Scholar 

  • Han Q, Zhang J, Li H, Luo Z, Ziaf K, Ouyang B, Wang T, Ye Z (2012) Identification and expression pattern of one stress-responsive NAC gene from Solanum lycopersicum. Mol Biol Rep 39(2):1713–1720

    Article  CAS  PubMed  Google Scholar 

  • 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(6):903–916

    Article  CAS  PubMed  Google Scholar 

  • Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53(3):383–397

    Article  CAS  PubMed  Google Scholar 

  • Hu H, Dai M, Yao J, **ao B, Li X, Zhang Q, **ong 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(35):12987–12992

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Johnson PF, Sterneck E, Williams SC (1993) Activation domains of transcriptional regulatory proteins. J Nutr Biochem 4(7):386–398

    Article  CAS  Google Scholar 

  • Kikuchi K, Ueguchi-Tanaka M, Yoshida K, Nagato Y, Matsusoka M, Hirano HY (2000) Molecular analysis of the NAC gene family in rice. Mol General Genet MGG 262(6):1047–1051

    Article  CAS  Google Scholar 

  • Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18(4):263–276

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 Molecular Biology Reporter 27(3):292–297

    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(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • 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(2):289–305

    Article  CAS  PubMed  Google Scholar 

  • Lu M, Ying S, Zhang D-F, Shi Y-S, Song Y-C, Wang T-Y, Li Y (2012) A maize stress-responsive NAC transcription factor, ZmSNAC1, confers enhanced tolerance to dehydration in transgenic Arabidopsis. Plant Cell Rep 31(9):1701–1711

    Article  CAS  PubMed  Google Scholar 

  • Mao X, Zhang H, Qian X, Li A, Zhao G, **g R (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63(8):2933–2946

    Article  PubMed Central  CAS  PubMed  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(3):352–359

    Article  CAS  Google Scholar 

  • Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19(1):270–280

    Article  PubMed Central  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(16):6309–6314

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nakashima K, Tran LSP, 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(4):617–630

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149(1):88–95

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms 1819(2):97–103

    Google Scholar 

  • Nicot N, Hausman J-F, Hoffmann L, Evers D (2005) Housekee** gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56(421):2907–2914

    Article  CAS  PubMed  Google Scholar 

  • Nogueira FT, Schlögl PS, Camargo SR, Fernandez JH (2005) SsNAC23, a member of the NAC domain protein family, is associated with cold, herbivory and water stress in sugarcane. Plant Sci 169(1):93–106

    Article  CAS  Google Scholar 

  • 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(1):30–44

    Article  CAS  PubMed  Google Scholar 

  • 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(2):135–139

    Article  CAS  PubMed  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) DNA-binding specificity and molecular functions of NAC transcription factors. Plant Sci 169(4):785–797

    Article  CAS  Google Scholar 

  • Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10(6):239–247

  • Pan Y, Seymour GB, Lu C, Hu Z, Chen X, Chen G (2012) An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. Plant Cell Rep 31(2):349–360

    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 

  • 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(5):707–719

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55(407):2343–2351

    Article  CAS  PubMed  Google Scholar 

  • Skriver K, Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O’Shea C (2010) The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signaling. Biochem J 426:183–196

    Article  PubMed  Google Scholar 

  • Song S-Y, Chen Y, Chen J, Dai X-Y, Zhang W-H (2011) Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. Planta 234(2):331–345

    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(2):159–170

    Article  CAS  PubMed  Google Scholar 

  • Sperotto RA, Ricachenevsky FK, Duarte GL, Boff T, Lopes KL, Sperb ER, Grusak MA, Fett JP (2009) Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230(5):985–1002

    Article  CAS  PubMed  Google Scholar 

  • Takada S, Hibara K, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128(7):1127–1135

    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(3):173–183

    Article  CAS  PubMed  Google Scholar 

  • Tang Y, Liu M, Gao S, Zhang Z, Zhao X, Zhao C, Zhang F, Chen X (2012) Molecular characterization of novel TaNAC genes in wheat and overexpression of TaNAC2a confers drought tolerance in tobacco. Physiol Plant 144(3):210–224

    Article  CAS  PubMed  Google Scholar 

  • 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(9):2481–2498

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tran LSP, Quach TN, Guttikonda SK, Aldrich DL, Kumar R, Neelakandan A, Valliyodan B, Nguyen HT (2009) Molecular characterization of stress-inducible GmNAC genes in soybean. Mol Genet Genomics 281(6):647–664

    Article  CAS  PubMed  Google Scholar 

  • Tran LSP, Nishiyama R, Yamaguchi-Shinozaki K, Shinozaki K (2010) Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops 1(1):32–39

    Article  PubMed  Google Scholar 

  • Uppalapati SR, Ishiga Y, Wangdi T, Urbanczyk-Wochniak E, Ishiga T, Mysore KS, Bender CL (2008) Pathogenicity of Pseudomonas syringae pv. tomato on tomato seedlings: phenotypic and gene expression analyses of the virulence function of coronatine. Mol Plant Microbe Interact 21(4):383–395

    Article  CAS  PubMed  Google Scholar 

  • **e Q, Frugis G, Colgan D, Chua N-H (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14(23):3024–3036

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang R, Deng C, Ouyang B, Ye Z (2011) Molecular analysis of two salt-responsive NAC-family genes and their expression analysis in tomato. Mol Biol Rep 38(2):857–863

    Article  CAS  PubMed  Google Scholar 

  • Zeller G, Henz SR, Widmer CK, Sachsenberg T, Rätsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58(6):1068–1082

    Article  CAS  PubMed  Google Scholar 

  • 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 55:119–135

    Google Scholar 

  • Zouine M, Latché A, Rousseau C, Regad F, Pech J-C, Philippot M, Bouzayen M, Delalande C, Frasse P, Schiex T (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  Google Scholar 

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Acknowledgments

This work was supported by National Natural Science Foundation of China (31101546), Natural Science Foundation of Chongqing of China (CSTC, 2011BB1068), and the Fundamental Research Funds for the Central Universities (CDJXS10230006).

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Authors and Affiliations

  1. Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Bioengineering College, Chongqing University, Campus A, Room 313, 174 Sha**ba Main Street, Chongqing, 400044, People’s Republic of China

    Mingku Zhu, Shuang Zhou, Lingling Wang, Tingting Dong & Yu Pan

  2. Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Bioengineering College, Chongqing University, Campus A, Room 204, 174 Sha**ba Main Street, Chongqing, 400044, People’s Republic of China

    Zongli Hu & Guo** Chen

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  1. Mingku Zhu
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  2. Zongli Hu
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  3. Shuang Zhou
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  4. Lingling Wang
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Correspondence to Guo** Chen.

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Zhu, M., Hu, Z., Zhou, S. et al. Molecular Characterization of Six Tissue-Specific or Stress-Inducible Genes of NAC Transcription Factor Family in Tomato (Solanum lycopersicum). J Plant Growth Regul 33, 730–744 (2014). https://doi.org/10.1007/s00344-014-9420-6

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