The abiotic stress-responsive NAC-type transcription factor SlNAC4 regulates salt and drought tolerance and stress-related genes in tomato (Solanum lycopersicum)

Plant Cell Reports

Volumn 33, Issue 11, 2014, Pages 1851-1863

  Zhu, Mingku ^a   Chen, Guoping ^a   Zhang, Jianling ^a   Zhang, Yanjie ^a   Xie, Qiaoli ^a   Zhao, Zhiping ^a   Pan, Yu ^a   Hu, Zongli ^a  

^a CHONGQING UNIVERSITY   (China)

Author keywords

Abiotic stress; Hormone; NAC transcription factor; SlNAC4; Tomato

Indexed keywords

ABSCISIC ACID; ACETIC ACID DERIVATIVE; CYCLOPENTANE DERIVATIVE; JASMONIC ACID METHYL ESTER; OXYLIPIN; PHYTOHORMONE; SMALL INTERFERING RNA; SODIUM CHLORIDE; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ADAPTATION; DNA MICROARRAY; DROUGHT; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLANT LEAF; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SHOOT; TOMATO; TRANSGENIC PLANT;

ABSCISIC ACID; ACETATES; ADAPTATION, PHYSIOLOGICAL; CYCLOPENTANES; DROUGHTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYLIPINS; PLANT GROWTH REGULATORS; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANT SHOOTS; PLANTS, GENETICALLY MODIFIED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, SMALL INTERFERING; SODIUM CHLORIDE; TRANSCRIPTION FACTORS;

EID: 84939879251     PISSN: 07217714     EISSN: 1432203X     Source Type: Journal    
DOI: 10.1007/s00299-014-1662-z     Document Type: Article

References (60)

1. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
2. 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 Coi1Mutant of Arabidopsis. Plant Physiol 116:1037–1042
3. Bussink HJ, Oliver R (2001) Identification of two highly divergent catalase genes in the fungal tomato pathogen, Cladosporium fulvum. Eur J Biochem 268:15–24
4. Chen G, Hu Z, Grierson D (2008) Differential regulation of tomato ethylene responsive factor LeERF3b, a putative repressor, and the activator Pti4 in ripening mutants and in response to environmental stresses. J Plant Physiol 165:662–670
5. Cuartero J, Bolarin M, Asins M, Moreno V (2006) Increasing salt tolerance in the tomato. J Exp Bot 57:1045–1058
6. Dhanda S, Sethi G (1998) Inheritance of excised-leaf water loss and relative water content in bread wheat (Triticum aestivum). Euphytica 104:39–47
7. Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
8. Dombrowski JE (2003) Salt stress activation of wound-related genes in tomato plants. Plant Physiol 132:2098–2107
9. 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
10. 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
11. Godoy JA, Pardo JM, Pintor-Toro JA (1990) A tomato cDNA inducible by salt stress and abscisic acid: nucleotide sequence and expression pattern. Plant Mol Biol 15:695–705
12. Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612
13. 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 39:1713–1720
14. 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
15. 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. Proc Natl Acad Sci 103:12987–12992
16. Jeong JS, Kim YS, Baek KH, Jung H, Ha S-H, Do Choi Y, Kim M, Reuzeau C, Kim J-K (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197
17. Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:D1182–D1187
18. Kaveh H, Nemati H, Farsi M, Jartoodeh S (2011) How salinity affect germination and emergence of tomato lines. J Biol Environ Sci 5:159–163
19. Kavi Kishor P, Zonglie H, Miao G-H, Hu C-A, Verma DPS (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394
20. Kavroulakis N, Papadopoulou KK, Ntougias S, Zervakis GI, Ehaliotis C (2006) Cytological and other aspects of pathogenesis-related gene expression in tomato plants grown on a suppressive compost. Ann Bot 98:555–564
21. Kim S-G, Kim S-Y, Park C-M (2007) A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226:647–654
22. 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 18:263–276
23. Lee JT, Prasad V, Yang PT, Wu JF, David Ho TH, Charng YY, Chan MT (2003) Expression of arabidopsis CBF1 regulated by an ABA/stress inducible promoter in transgenic tomato confers stress tolerance without affecting yield. Plant Cell Environ 26:1181–1190
24. Lim CJ, Kim WB, Lee B-S, Lee HY, Kwon T-H, Park JM, Kwon S-Y (2010) Silencing of SlFTR-c, the catalytic subunit of ferredoxin: thioredoxin reductase, induces pathogenesis-related genes and pathogen resistance in tomato plants. Biochem Biophys Res Commun 399:750–754
25. −ΔΔCT method. Methods 25:402–408
26. 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
27. Lu C, Li Y, Chen A, Li L, Zuo J, Tian H, Luo Y, Zhu B (2013) LeERF1 improves tolerance to drought stress in tomato (Lycopersicon esculentum) and activates downstream stress-responsive genes. Afr J Biotechnol 9:6294–6300
28. 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. Physiol Plant 149:474–486
29. Najami N, Janda T, Barriah W, Kayam G, Tal M, Guy M, Volokita M (2008) Ascorbate peroxidase gene family in tomato: its identification and characterization. Mol Genet Genomics 279:171–182
30. 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 51:617–630
31. Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in arabidopsis and grasses. Plant Physiol 149:88–95
32. Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103
33. Nicot N, Hausman J-F, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56:2907–2914
34. 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 169:93–106
35. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005a) DNA-binding specificity and molecular functions of NAC transcription factors. Plant Sci 169:785–797
36. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005b) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87
37. Orellana S, Yanez M, Espinoza A, Verdugo I, Gonzalez E, Ruiz-Lara S, Casaretto JA (2010) The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant Cell Environ 33:2191–2208
38. 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 31:349–360
39. Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381
40. Qin F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52:1569–1582
41. 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 234:331–345
42. 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
43. 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
44. 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 144:210–224
45. 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 16:2481–2498
46. 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 281:647–664
47. 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 1:32–39
48. Wang J, Zhang H, Allen RD (1999) Overexpression of an arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant Cell Physiol 40:725–732
49. Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313
50. Wu Y, Deng Z, Lai J, Zhang Y, Yang C, Yin B, Zhao Q, Zhang L, Li Y, Yang C (2009) Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res 19:1279–1290
51. Xie Q, Frugis G, Colgan D, Chua N-H (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036
52. Xiong L, Ishitani M, Zhu J-K (1999) Interaction of osmotic stress, temperature, and abscisic acid in the regulation of gene expression in Arabidopsis. Plant Physiol 119:205–212
53. 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
54. Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2009) Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic arabidopsis. Planta 229:1065–1075
55. Zegzouti H, Jones B, Marty C, Lelievre J-M, Latché A, Pech J-C, Bouzayen M (1997) ER5, a tomato cDNA encoding an ethylene-responsive LEA-like protein: characterization and expression in response to drought, ABA and wounding. Plant Mol Biol 35:847–854
56. Zhang C, Liu J, Zhang Y, Cai X, Gong P, Zhang J, Wang T, Li H, Ye Z (2011) Overexpression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. Plant Cell Rep 30:389–398
57. 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
58. Zhong R, Lee C, Ye Z-H (2010) Global analysis of direct targets of secondary wall NAC master switches in arabidopsis. Mol Plant 3:1087–1103
59. Zhu M, Chen G, Zhou S, Tu Y, Wang Y, Dong T, Hu Z (2014a) 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
60. Zhu M, Hu Z, Zhou S, Wang L, Dong T, Pan Y, Chen G (2014b) Molecular characterization of six tissue-specific or stress-inducible genes of NAC transcription factor family in tomato (Solanum lycopersicum). J Plant Growth Regul:1–15