Browse > Article
http://dx.doi.org/10.5010/JPB.2017.44.1.001

Biological roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in solanaceous crops  

Tweneboah, Solomon (Department of Applied Biology, College of Agriculture & Life Sciences, Chungnam National University)
Oh, Sang-Keun (Department of Applied Biology, College of Agriculture & Life Sciences, Chungnam National University)
Publication Information
Journal of Plant Biotechnology / v.44, no.1, 2017 , pp. 1-11 More about this Journal
Abstract
Evolutionary studies conducted on NAC (NAM, ATAF1&2, and CUC2) genes for all major groups of land plants, indicate the presence of the NAC subfamilies, even in the early land plants. The varied roles played by NAC proteins in plant growth and development range from the formation of shoot apical meristem, floral organ development, reproduction, lateral shoot development, and defense responses to biotic and abiotic stresses. Considering the value and importance of solanaceous crops, the study of NAC proteins in these plants needs to be intensified. This will help to identify and functionally characterize their promoters, which will subsequently aid in engineering plants with improved performance under stressful conditions. In this review, the functionally characterized NAC transcription factors specific to tomato, potato, tobacco, chili pepper and eggplant (aubergine) are summarized, clearly indicating their biological functions in the defense mechanism of the plants, against biotic and abiotic stresses.
Keywords
NAC transcription factors; Solanaceous crops; Biotic and abiotic stresses;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Weizao Huang W, Miao M, Joanna Kud J, Niu X, Ouyang B, Zhang J, Ye Z, Kuhl JC, Yongsheng Liu Y, Xiao F (2013) SlNAC1, a stress-related transcription factor, is fine-tuned on both the transcriptional and the post-translational level. New Phytologist 197:1214-1224   DOI
2 Kaneda T, Taga Y, Takai R, Iwano M, Matsui H, Takayama S, Isogai A, Che FS (2009) The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death
3 Kikuchi K, Ueguchi-Tanaka M, Yoshida KT, Nagato Y, Matsusoka M, Hirano HY (2000) Molecular analysis of the NAC gene family in rice. Mol Gen Genet 262:1047-1051   DOI
4 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 19:1279-1290   DOI
5 Xu Q, He Q, Li S, Tian Z (2014) Molecular characterization of StNAC2 in potato and its overexpression confers drought and salt tolerance. Acta Physiol Plant 36:1841   DOI
6 Xu ZY, Kim SY, Hyeon DY, Kim DH, Dong T, Park Y, Jin JB, Joo SH, Kim SK, Hong JC, Hwang D, Hwang I (2013). The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell 25 4708-4724   DOI
7 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 38:857-863   DOI
8 Yoshii M, Shimizu T, Yamazaki M, Higashi T, Miyao A, Hirochika H, Omura T (2009) Disruption of a novel gene for a NAC-domain protein in rice confers resistance to Rice dwarf virus. Plant J 57:615-625   DOI
9 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   DOI
10 You J, Zhang L, Song B, Qi X, Chan Z (2015) Systematic Analysis and Identification of Stress-Responsive Genes of the NAC Gene Family in Brachypodium distachyon. PLos ONE 10: e0122027   DOI
11 Weese TL, Bohs L (2007) A three-gene phylogeny of the genus Solanum (Solanaceae) Syst Bot 32:445-463   DOI
12 Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18:263-276   DOI
13 Kim S, Park M, Yeom SI, Kim YM, Lee JM, Lee HA, Seo E, Choi J, Cheong K, Kim KT, Jung K, Lee GW, Oh SK, Bae C, Kim SB, Lee HY, Kim SY, Kim MS, Kang BC et al (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nature Genetics 46:270-280   DOI
14 Kleinow T, Himbert S, 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 Science 177:360-370   DOI
15 Knapp S (2002) Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. J Exp Botany 53: 2001-2022   DOI
16 Li XD, Zhuang KY, Liu ZM, Yang DY, Ma NN, Meng QW (2016) Overexpression of a novel NAC-type tomato transcription factor, SlNAM1, enhances the chilling stress tolerance of transgenic tobacco. J Plant Physiol 204:54-65   DOI
17 Liang XQ, Ma NN, Wang GD, Meng X, Ai XZ, Meng QW (2015) Suppression of SlNAC1 reduces heat resistance in tomato plants. Biol Plant 59:92-98   DOI
18 Liu B, Ouyang Z, Zhang Y, Li X, Hong Y, Huang L, Liu S, Zhang H, Li D, Song F (2014) Tomato NAC transcription factor SlSRN1 positively regulates defense response against biotic stress but negatively regulates abiotic stress response. PLoS ONE 9: e102067   DOI
19 Zheng XY, Spivey NW, Zeng W, Liu PP, Fu ZQ, Klessig DF, He SY, Dong X (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe. 11:587-596   DOI
20 Zhao D, Derkx AP, Liu DC, Buchner P, Hawkesford MJ (2015) Overexpression of a NAC transcription factor delays leaf senescence and increases grain nitrogen concentration in wheat. Plant Biol (Stuttg). 17:904-913   DOI
21 Sun L, Zhang H, L, D, Huang L, Hong Y, Ding XS, Nelson RS, Zhou X, Song F (2013) Functions of rice NAC transcriptional factors, ONAC122 and ONAC131, in defense responses against Magnaporthe grisea. Plant Mol Biol 81:41-56   DOI
22 Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739   DOI
23 Puranik S, Sahu PP, Srivastava PS, Prasad M (2012). NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369-381   DOI
24 Olmstead RG, Bohs L, Migid HA, Santiago-Valentin E, Garcia VF, Collier SM (2008) A molecular phylogeny of the Solanaceae. Taxon 57:1159-1181
25 Ulm R, Baumann A, Oravecz A, Mate Z, Adam E, Oakeley EJ, Schafer E, Nagy F (2004) Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc Natl Acad Sci USA 101:1397-1402   DOI
26 Wang G, Zhang S, Ma X, Wang Y, Kong F, Meng Q (2016) A stress-associated NAC transcription factor (SlNAC35) from tomato plays a positive role in biotic and abiotic stresses. Physiologia Plantarum 158:45-64   DOI
27 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 22:1227-1238   DOI
28 Zou C, Sun K, Mackaluso JD, Seddon AE, Jin R, Thomashow MF, Shiu SH (2011) Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana. Proc. Nat. Acad. Sci. USA 108:14992-14997   DOI
29 Olsen AN, Erns, HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:1360-1385
30 Portis E, Barchi L, Toppino L, Lanteri S, Acciarri N, Felicioni N, Fusari F, Barbierato V, Cericola F, Vale G, Rotino GL (2014) QTL mapping in eggplant reveals clusters of yield-related loci and orthology with the tomato genome. PLoS ONE 9:e89499   DOI
31 Rushton PJ, Bokowiec MT, Han S, Zhang HH, Brannock JF, Chen X, Laudeman TW, Timko MP (2008) Tobacco transcription factors: novel insights into transcriptional regulation in the solanaceae. Plant Physiol 147:280-295   DOI
32 Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci. 15:247-258   DOI
33 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   DOI
34 Saga H, Ogawa T, Kai K, Suzuki H, Ogata Y, Sakurai N, Shibata D, Ohta D (2012) Identification and characterization of ANAC042, a transcription factor family gene involved in the regulation of camalexin biosynthesis in Arabidopsis. Mol Plant Microbe Interact 25:684-696   DOI
35 Sarkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evol Biol 13:214   DOI
36 Selth LA, Dogra SC, Rasheed MS, Healy H, Randles JW, Rezaian MA (2005) A NAC domain protein interacts with tomato leaf curl virus replication accessory protein and enhances viral replication. Plant Cell 17:311-325   DOI
37 Ma HL, Zhou HL, Zhang HY, Zhao J (2010) Cloning and expression analysis of an AP2/ERF gene and its responses to phytohormones and abiotic stresses in rice. Rice Sci 17:1-9   DOI
38 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 63:289-305
39 Lv X, Lan S, Guy KM, Yang J, Zhang M, Hu Z (2016) Global Expressions Landscape of NAC Transcription Factor Family and Their Responses to Abiotic Stresses in Citrullus lanatus. Scientific Reports 6:30574   DOI
40 Ma NN, Zuo YQ, Liang XQ, Yin B, Wang GD, Meng QW (2013) The multiple stress-responsive transcription factor SlNAC1 improves the chilling tolerance of tomato. Physiologia Plantarum 149:474-486   DOI
41 Ma N, Feng H, Meng X, Li D, Yang D, Wu C, Meng Q (2014) Overexpression of tomato SlNAC1 transcription factor alters fruit pigmentation and softening. BMC Plant Biol 14:351   DOI
42 Matsusoka M, Hirano HY (2000) Molecular analysis of the NAC gene family in rice. Mol Gen Genet 262:1047-1051   DOI
43 Meng C, Yang D, Ma X, Zhao W, Liang X, Ma N, Meng Q (2016) Suppression of tomato SlNAC1 transcription factor delays fruit ripening. J Plant Physiol 193:88-96   DOI
44 Na C, Shuanghua W, Jinglong F, Bihao C, Jianjun L, Changming C, Jin J (2016) Overexpression of the eggplant (Solanum melongena) NAC family transcription factor SmNAC suppresses resistance to bacterial wilt. Scientific Reports 6:31568   DOI
45 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   DOI
46 Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. BBA 1819:97-103
47 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   DOI
48 Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS (2013) Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res 20:403-423   DOI
49 Smekalova V, Doskocilova A, Komis G, Samaj J (2013) Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol Advances 32:2-11
50 Song FY, Su HY, Cheng XH, Zhu LY, Wang L (2015) Characterization and expression analysis of TNAC genes of tomato. Bull Bot Res 35:898-903
51 Stern S, de Fatima Agra M, Boh, L (2011) Molecular delimitation of clades within New World species of "spiny solanums" (Solanum subg. Leptostemonum) Taxon 60:1429-1441
52 Cenci A, Guignon V, Roux N, Rouard M (2014) Genomic analysis of NAC transcription factors in banana (Musa acuminata) and definition of NAC orthologous groups for monocots and dicots. Plant Mol Biol 85:63-80   DOI
53 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 46:521-529   DOI
54 Oh SK, Lee S, Yu SH, Choi D (2005) Expression of a novel NAC domain-containing transcription factor (CaNAC1) is preferentially associated with incompatible interactions between chili pepper and pathogens. Planta 222:876-887   DOI
55 Nakashima K, Tran LP, Nguyen DV, 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 51:617-630   DOI
56 Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4:248
57 Nuruzzaman M, Sharoni AM, Satoh K, Karim MR, Harikrishna JA, Shimizu T, Sasaya T, Omura T, Haque MA, Hasan SMZ, Ahmad A, Kikuchi S (2015) NAC transcription factor family genes are differentially expressed in rice during infections with Rice dwarf virus, Rice black-streaked dwarf virus, Rice grassy stunt virus, Rice ragged stunt virus, and Rice transitory yellowing virus. Front Plant Sci 6:676
58 Duval M, Hsieh TF, Kim SY, Thomas TL (2002) Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Molecular Biology 50:237-248   DOI
59 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 43:745-757   DOI
60 Du M, Zhi Q, Deng L, Li S, Li H, Yan L, Huang Z, Wang B, Jiang H, Huang T, Li CB, Wei J, Kang L, Li J, Li C (2014) Closely related NAC transcription factors of tomato differentially regulate stomatal closure and reopening during pathogen attack. Plant Cell 26:3167-3184   DOI
61 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 Genet Genomics 280:547-563   DOI
62 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   DOI
63 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   DOI
64 Fu Y, Guo H, Cheng Z, Wang R, Li G, Huo G, Liu W (2013) NtNAC-R1, a novel NAC transcription factor gene in tobacco roots, responds to mechanical damage of shoot meristem. Plant Physiol Biochem 69:74-81   DOI
65 Han QQ, Qiao P, Song YZ, Zhang JY (2015) Structural analysis and tissue-specific expression patterns of a novel salt-inducible NAC transcription factor gene from Nicotiana tabacum cv. Xanthi. J Hortl Sci Biotechnol 89:700-706
66 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   DOI
67 Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr Opin Plant Biol 4:301-308   DOI
68 Griffiths AJF, Wessler SR, Lewontin RC, Gelbart WM, Suzuki DT, Miller JH (2005) An Introduction to Genetic Analysis (8th edition). New York: New York: WH Freeman; Basingstoke: Palgrave. pp 301-339
69 Guo WL, Wang SB, Chen RG, Chen BH, Du XH, Yin YX, Gong ZH, Zhang YY (2015) Characterization and expression profile of CaNAC2 pepper gene. Front Plant Sci 6:755
70 Han Q, Zhang J, Li H, Luo Z, Ziaf K, Ouyang B, Wang T, Ye Z (2012) Identification and expression pattern of one stressresponsive NAC gene from Solanum lycopersicum. Mol Biol Rep. 39:1713-1720   DOI
71 Han QQ, Song YZ, Zhang JY, Liu L F (2014) Studies on the role of the SlNAC3 gene in regulating seed development in tomato (Solanum lycopersicum). J Hortl Sci Biotechnol 89:423-429   DOI
72 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 Biology 10:145   DOI
73 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   DOI
74 Hernandez-Garcia CM and Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Science 217-218:109-119   DOI
75 Hirota A, Kato T, Fukaki H, Aida M, Tasaka M (2007) The auxin-regulated AP2/EREBP gene PUCHI is required for morphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell 19:2156-2168   DOI
76 Jin JP, Zhang H, Kong L, Gao G, Luo JC (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:D1182-D1187   DOI
77 Zhu T, Nevo E, Sun D, Peng J (2012) Phylogenetic analyses unravel the evolutionary history of NAC proteins in plants. Evolution 66:1833-1848   DOI
78 Zhu M, Hu Z, Zhou S, Wang L, Dong T, Pan Y, Chen G (2014a) Molecular Characterization of Six Tissue-Specific or Stress-Inducible Genes of NAC Transcription Factor Family in Tomato (Solanum lycopersicum). J Plant Growth Regulation 33:730-744   DOI
79 Zhu M, Chen G, Zhang J, Zhang Y, Xie Q, Zhao Z, Pan Y, Hu Z (2014b) The abiotic stress-responsive NAC-type transcription factor SlNAC4 regulates salt and drought tolerance and stress-related genes in tomato (Solanum lycopersicum). Plant Cell Rep. 33:1851-1863   DOI
80 Zhu M, Chen G, Zhou S, Tu Y, Wang Y, Dong T, Hu Z (2014c) 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   DOI