Abstract
The NAC family is considered one of the largest plant-specific transcription factors families, and functions in diverse and vital physiological processes during development. In the present study, we performed a complete bioinformatics analysis of the NAC family transcription factors in tomato, and annotated the non-redundant SlNAC1-74 proteins into 12 subgroups. Six NAC genes from tomato, which were designated SNAC4–SNAC9, were studied instensively. The expression analysis indicated that each SNAC gene exhibited a specific expression pattern in the tissues examined. SNAC4 and SNAC6 were most highly expressed in the stems and leaves, whereas the expression levels of SNAC5, SNAC8 and SNAC9 were higher in young leaves and old leaves, respectively. In addition, the expression patterns of SNAC genes were characterized during the development of tomato fruits. All of the genes were further investigated to determine their responsiveness to hormones, and a coordinated expression was observed. The expression of the SNAC gene transcripts was induced by ABA, SA and short-time ethylene treatment, whereas their transcription was inhibited by GA, 6-BA and IAA. Our present study provides a useful reference for future investigations of NAC genes in tomato and other fleshy fruits.
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Reference
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
Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055
Beaudoin N, Serizet C, Gosti (2000) Interactions between abscisic acid and ethylene signaling acscades. The Plant Cell 12:1103–1115
Bouzayen M (2002) Ripening- associated transcriptional regulation in the tomato. A case of cross- talk between ethylene and auxin. Comparative Biochemistry and Physiology, Part A: Molecular and Integrative. Physiology 132:S97
Brecht JK (1987) Locular gel formation in developing tomato fruit and initiation of ethylene production. Hortscience 22(3):476–479
Bu Q, Jiang H, Li CB, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Li C (2008) Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res 18:756–767
Carbonell-Bejerano P, Urbez C, Carbonell J, Granell A, Perez-Amador MA (2010) A fertilization-independent developmental program triggers partial fruit development and senescence processes in pistills of Arabidopsis. Plant Physiol 154:163–172
Causier B, Ashworth M, Guo W, Davies B (2012) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158:423–438
Civello PM, Powell AL, Sabehat A (1999) An expansion gene expressed in ripening strawberry fruit. Plant Physiol 121:1273–1279
Duval M, Hsieh TF, Kim SY, Thomas TL (2002) Molecular characterization of AtNAM: a member of the Arabidopsis NACdomain superfamily. Plant Mol Biol 50:237–248
Ernst HA, Olsen AN, Skriver K, Larsen S, Lo Leggio L (2004) Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep 5:297–303
Fang Y, You J, Xie K, Xie W, Xiong L (2008) Systematic sequence analysis and identification of tissue-specificor stress-responsive genes of NAC transcription factor family in rice. Mol Gen Genomics 280:547–563
Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, 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
Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell Online 16(suppl 1):S170–S180
Guilherme LP, Carolina SM, Maximiller DC, Pedro AR, Murilo SA, Claudine MC, Luciano GF, Elizabeth PF (2009) Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444:10–23
Guo YF, Gan SS (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612
Han QQ, Zhang JH, Li HX, Luo ZD, KhurramZiaf WTT, Ye ZB (2012) Identification and expression pattern of one stress-responsive NAC gene from Solanum lycopersicum. Mol Biol Rep 39:1713–1720
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 44:903–916
He YH, Gan SS (2002) A gene encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis. Plant Cell 14:805–815
Hu HH, Dai MQ, Yao JL, Xiao BZ, Li XH, Zhang QF, Xiong LZ (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci 103:12987–12992
Hu HH, You J, Fang YJ, Zhu XY, Qi ZY, Xiong LZ (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181
Huang H, Wang Y, Wang S, Wu X, Yang K, Niu Y, Dai SL (2012) Transcriptome-wide survey and expression analysis of stress-responsive NAC genes in Chrysanthemum lavandulifolium. Plant Sci 193:18–27
International Tomato Genome Sequencing Project (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
Jeong JS, Kim YS, Baek KH, Hairn J, Ha SH, Choi YD, Minkyun K, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiologyl 153:185–197
Jing HC, Schippers JHM, Hille J, Dijkwel PP (2005) Ethylene-induced leaf senescence depends on age-related changes and OLD genes in Arabidopsis. J Exp Bot 56:2915–2923
Josph R, Eliahu G, Yang SF (1990) Characterization of abscisic acid-induced ethylene production in citrus leaf and tomato fruit tissues. Plant Physiol 92:48–53
Kende H, Zeevaart JAD (1997) The five classical plant hormones. Plant Cell 9:1197–1210
Kim SG, Kim SY, Park CM (2007a) A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226:647–654
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 Journal 55(1):77–88
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 35:203–213
Kim YS, Kim SG, Park JE (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18:3132–3144
Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59
Ko JH, Yang SH, Park AH, Lerouxel O, Han KH (2007) ANAC012, a member of the plant-specific NAC transcription factor family, negatively regulates xylary fiber development in Arabidopsis thaliana. Plant J 50:1035–1048
Kou XH, Watkins CB, Gan SS (2012) Arabidopsis AtNAP regulates fruit senescence. J Exp Bot 63:6139–6147
Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860
Li LB, Zhang YR, Liu KC, Ni ZF, Fang ZJ, Sun QX, Gao JW (2010) Identification and bioinformatics analysis of SnRK2 and CIPK family genes in sorghum. Agric Sci China 9:19–30
Lin HN, Zhu W, Silva CJ, Gu X, Buell CR (2006) Intron gain and loss in segmentally duplicated genes in rice. Genome Biol 7:R41
Lin R, Zhao W, Meng X, Wang M, Peng Y (2007) Rice gene OsNAC19 encodes a novel NAC-domain transcription factor and responds to infection by Magnaporthe grisea. Plant Sci 172:120–130
Liu YZ, Baig MN, 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 27:292–297
Manoj K, Srivastava UN (2000) Delayed ripening of banana fruit by salicylic acid. Plant Sci 158:87–96
Mao C, Ding W, Wu Y, Yu J, He X, Shou H, Wu P (2007) Overexpression of a NAC-domain protein promotes shoot branching in rice. New Phytol 176:288–298
Martinez GA, Chaves AR, Anon MC (1996) Effect of exogenous application of gibberellic acid on color change and phenylalanine ammonia-lyase, chlorophyllase, and peroxidase activities during ripening of strawberry fruit (Fragaria × ananassa Duch.). J Plant Growth Regul 15:139–146
Meng Q, Zhang C, Gai J, Yu D (2007) Molecular cloning, sequence characterization and tissue-specific expression of six NAC-like genes in soybean (Glycine max (L.) Merr.). J Plant Physiol 164:1002–1012
Nuruzzaman M, Gupta M, Zhang CJ, Wang L, Xie WB, Xiong LZ, Zhang QF, Lian XM (2008) Sequence and expression analysis of the thioredoxin protein gene family in rice. Mol Gen Genomics 280:139–151
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 465:30–44
Oeller PW, Lu MW, Taylor LP, Pike DA, Theologis A (1991) Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254:437–439
Ogo Y, Kobayashi T, Nakanishi-Itai R, Nakanishi H, Kakei Y, Takahashi M, Toki S, Mori S, Nishizawa NK (2008) A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. J Biol Chem 283:13407–13417
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. Gene Genet Syst 80:135–139
Olsen AN, Ernst HA, Leggio LL (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87
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 10:239–247
Peng H, Cheng HY, Yu XW, Shi QH, Zhang H, Li JG, Ma H (2009) Characterization of a chickpea (Cicerarietinum L.) NACfamily gene, CarNAC5, which is both developmentally- and stress-regulated. Plant Physiol Biochem 47:1037–1045
Sablowski RW, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103
Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature, differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol l3:217–223
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exprimental Bot 58:221–227
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
Sperotto RA (2009) Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230:985–1002
Tamura K, Dudley J, Nei M (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version4.0. Mol Biol Evol 24:1596–1599
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
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 earlyresponsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301
Watkins CB (2002) Ethylene synthesis, mode of action, consequences and control. In: Knee M (ed) Fruit quality and its biological basis. Sheffield Academic Press, Sheffield, pp 180–224
Weir I, Lu J, Cook H, Causier B, Schwarz SZ, Davies B (2004) CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum. Development 131:915–922
Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Gene Dev 14:3024–3036
Yamaguchi M, Kubo M, Fukuda H, Demura T (2008) Vascular related NAC-domain7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 55:652–664
Yoshii M, Yamazaki M, Rakwal R, Kishi-Kaboshi M, Miyao A, Hirochika H (2010) The NAC transcription factor RIM1 of rice is a new regulator of jasmonate signaling. Plant J 61:804–815
Zhang K, Xia X, Zhang Y, Gan SS (2012) An ABA-regulated and Golgi-localized protein phosphatase controls water loss during leaf senescence in Arabidopsis. Plant J 69:667–678
Zhong RQ, Richardson EA, Ye ZH (2007b) Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225:1603–1611
Zhong RQ, Ye ZH (2007) Regulation of cell wall biosynthesis. Curr Opin Plant Biol 10:564–572
Acknowledgements
This work was supported by the National Natural Science Foundation of China (project no. 31171769) and Postdoctoral Science Founding Special Foundation Project of China (project no. 201003300)
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Xiaohong Kou and Shuang Wang made equal contributions to this work.
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Kou, X., Wang, S., Wu, M. et al. Molecular Characterization and Expression Analysis of NAC Family Transcription Factors in Tomato. Plant Mol Biol Rep 32, 501–516 (2014). https://doi.org/10.1007/s11105-013-0655-3
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DOI: https://doi.org/10.1007/s11105-013-0655-3