Identification and characterization of a novel NAC-like gene in chrysanthemum (Dendranthema lavandulifolium)

Plant Cell Reports

Volumn 35, Issue 8, 2016, Pages 1783-1798

  Yang, Yanfang ^a,b   Zhu, Kai ^b   Wu, Jian ^b   Liu, Liqing ^c   Sun, Guiling ^d   He, Yanbiao ^d   Chen, Fadi ^b   Yu, Deyue ^b  

^a RESEARCH INSTITUTE OF FORESTRY   (China)

^b NANJING AGRICULTURAL UNIVERSITY   (China)

^c Fujian Provincial Key Lab of Subtropic Plant Physiology and Biochemistry   (China)

^d KUNMING INSTITUTE OF BOTANY   (China)

Author keywords

Abiotic stress; Chrysanthemum; NAC; Transcription factor

Indexed keywords

PLANT PROTEIN; SODIUM CHLORIDE; TRANSCRIPTION FACTOR;

ADAPTATION; AMINO ACID SEQUENCE; ANTIBODY SPECIFICITY; CELL FRACTIONATION; CHEMISTRY; CHRYSANTHEMUM; DNA SEQUENCE; DROUGHT; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE VECTOR; GENETIC TRANSFORMATION; GENETICS; METABOLISM; PHYLOGENY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENE; REAL TIME POLYMERASE CHAIN REACTION; SALT TOLERANCE; TOBACCO; TRANSCRIPTION INITIATION; TRANSGENIC PLANT;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; CHRYSANTHEMUM; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC VECTORS; ORGAN SPECIFICITY; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; REAL-TIME POLYMERASE CHAIN REACTION; SALT-TOLERANCE; SEQUENCE ANALYSIS, DNA; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; SUBCELLULAR FRACTIONS; TOBACCO; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSFORMATION, GENETIC;

EID: 84970998098     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-016-1996-9     Document Type: Article

References (67)

1. Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, Tripp J, Weber C, Zielinski D, von Koskull-Döring P (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29:471–487
2. Chen Y, Jiang JF, Song AP, Chen SM, Shan H, Luo HL, Gu CS, Sun J, Zhu L, Fang WM, Chen FD (2013) Ambient temperature enhanced freezing tolerance of Chrysanthemum dichrum CdICE1 Arabidopsis via miR398. BMC Biol 11:121
3. Dai F, Zhang C, Jiang X, Kang M, Yin X, Lü P, Zhang X, Zheng Y, Gao J (2012) RhNAC2 and RhEXPA4 are involved in the regulation of dehydration tolerance during the expansion of rose petals. Plant Physiol 160:2064–2082
4. Danquah A, Zelicourt AD, Colcombet J, Hirt H (2014) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32:40–52
5. Duval I, Lachance D, Giguère I, Bomal C, Morency MJ, Pelletier G, Boyle B, MacKay JJ, Séguin A (2014) Large-scale screening of transcription factor-promoter interactions in spruce reveals a transcriptional network involved in vascular development. J Exp Bot 65:2319–2333
6. Fang YJ, Xie KB, Xiong LZ (2014) Conserved miRNA164-targedted NAC genes negatively regulate drought resistance in rice. J Exp Bot 65:2119–2135
7. Fu JX, Wang Y, Huang H, Zhang C, Dai SL (2013) Reference gene selection for RT-qPCR analysis of Chrysanthemum lavandulifolium during its flowering stages. Mol Breed 31:205–215
8. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525
9. Ganesan G, Sankararamasubramanian HM, Harikrishnan M, Ganpudi A, Parida A (2012) A MYB transcription factor from the grey mangrove is induced by stress and confers NaCl tolerance in tobacco. J Exp Bot 63(12):4549-4561
10. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652
11. Guan QM, Yue XL, Zeng HT, Zhu JH (2014) The protein phosphatase RCF2 and its interacting partner NAC019 are critical for heat stress–responsive gene regulation and thermotolerance in Arabidopsis. Plant Cell 26:438–453
12. Hartmann L, Pedrotti L, Weiste C, Fekete A, Schierstaedt J, Göttler J, Kempa S, Krischke M, Dietrich K, Mueller MJ, Vicente-Carbajosa J, Hanson J, Dröge-Laser W (2015) Crosstalk between two bZIP signaling pathways orchestrates salt-induced metabolic reprogramming in Arabidopsis roots. Plant Cell 27:2244–2260
13. He HY, He LF, Gu MH (2014) Role of microRNAs in aluminum stress in plants. Plant Cell Rep 33:831–836
14. 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. Pro Natl Acad Sci USA 103:12987–12992
15. Huang H, Wang Y, Wang S, Wu X, Yang K, Niu Y, Dai S (2012) Transcriptome-wide survey and expression analysis of stress-responsive NAC genes in Chrysanthemum lavandulifolium. Plant Sci 193–194:18–27
16. Jensen MK, Hagedorn PH, de Torres-Zabala M, Grant MR, Rung JH, Collinge DB, Lyngkjaer MF (2008) Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signaling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. Plant J 56:867–880
17. Jiang G, Jiang X, Lü P, Liu J, Gao J, Zhang C (2014a) The Rose (Rosa hybrida) NAC transcription factor 3 gene, RhNAC3, involved in ABA signaling pathway both in rose and Arabidopsis. PLoS One 9:e109415
18. Jiang X, Zhang C, Lü P, Jiang G, Liu X, Dai F, Gao J (2014b) RhNAC3, a stress-associated NAC transcription factor, has a role in dehydration tolerance through regulating osmotic stress-related genes in rose petals. Plant Biotechnol J 12:38–48
19. Kato H, Motomura T, Komeda Y, Saito T, Kato A (2010) Overexpression of the NAC transcription factor family gene ANAC036 results in a dwarf phenotype in Arabidopsis thaliana. J Plant Physiol 167:571–577
20. 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
21. Laufs P, Peaucelle A, Morin H, Traas J (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131:4311–4322
22. Lindemose S, O’Shea C, Jensen MK, Skriver K (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci 14:5842–5878
23. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406
24. Liu LQ, Zhu K, Yang YF, Wu J, Chen FD, Yu DY (2008) Molecular cloning, expression profiling and trans-activation property studies of a DREB2-like gene from chrysanthemum (Dendranthema vestitum). J Plant Res 121:215–226
25. Liu QL, Xu KD, Zhao LJ, Pan YZ, Jiang BB, Zhang HQ, Liu GL (2011) Overexpression of a novel chrysanthemum NAC transcription factor gene enhances salt tolerance in tobacco. Biotechnol Lett 33:2073–2082
26. Liu QL, Zhong M, Li S, Pan YZ, Jiang BB, Jia Y, Zhang HQ (2013) Overexpression of a chrysanthemum transcription factor gene, DgWRKY3, in tobacco enhances tolerance to salt stress. Plant Physiol Biochem 69:27–33
27. Liu XF, Liang WH (2009) Localization analysis of GFP in onion epidermal cell via Agrobacterium tumefaciens-mediated transformation. J Henan Norm Univ (Nat Sci) 37(1):123–150 (In Chinese)
28. Mao XG, Chen SS, Li A, Zhai CC, Jing RL (2014) Novel NAC Transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances in Arabidopsis. PLoS One 9:e84359
29. Mehterov N, Balazadeh S, Hille J, Toneva V, Mueller-Roeber B, Gechev T (2012) Oxidative stress provokes distinct transcriptional responses in the stress-tolerant atr7 and stress-sensitive loh2 Arabidopsis thaliana mutants as revealed by multi-parallel quantitative real-time PCR analysis of ROS marker and antioxidant genes. Plant Physiol Biochem 59:20–29
30. Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665
31. Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170
32. 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
33. Naoki Y, Takanari I, Youichi K, Minami M, Hirohiko H, Masaki I, Oda K (2009) Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta 229:1065–1075
34. Olsen AN, Ernst HA, Lo Leggio L, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:1360–1385
35. Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247
36. Ruiz-Rerrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510
37. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258
38. Saad AS, Li X, Li HP, Huang T, Gao CS, Guo MW, Cheng W, Zhao GY, Liao YC (2013) A rice stress-responsive NAC gene enhances tolerance of transgenic wheat to drought and salt stresses. Plant Sci 203–204:33–40
39. 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
40. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309
41. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Pro Natl Acad Sci USA 103:18822–18827
42. Sato H, Mizoi J, Tanaka H, Maruyama K, Qin F, Osakabe Y, Morimoto K, Ohori T, Kusakabe K, Nagata M, Shinozaki K, Yamaguchi-Shinozaki K (2014) Arabidopsis DPB3-1, a DREB2A interactor, specifically enhances heat stress-induced gene expression by forming a heat stress-specific transcriptional complex with NF-Y subunits. Plant Cell 26:4954–4973
43. Shahnejat-Bushehri S, Mueller-Roeber B, Balazadeh S (2012) Arabidopsis NAC transcription factor JUNGBRUNNEN1 affects thermomemory-associated genes and enhances heat stress tolerance in primed and unprimed conditions. Plant Signal Behavor 7:1518–1521
44. Shibuya K, Shimizu K, Niki T, Ichimura K (2014) Identification of a NAC transcription factor, EPHEMERAL1, that controls petal senescence in Japanese morning glory. Plant J 79:1044–1051
45. 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 3:217–223
46. Song A, Zhu X, Chen F, Gao H, Jiang J, Chen S (2014) A chrysanthemum heat shock protein confers tolerance to abiotic stress. Int J Mol Sci 15:5063–5078
47. Stief A, Altmann S, Hoffmann K, Pant BD, Scheible WR, Bäurle I (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26:1792–1807
48. Sun J, Ren L, Cheng Y, Gao J, Dong B, Chen S, Chen F, Jiang J (2014) Identification of differentially expressed genes in Chrysanthemum nankingense (Asteraceae) under heat stress by RNA seq. Gene 552:59–66
49. Sunkar R, Chinnusamy V, Zhu JH, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:1360–1385
50. Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25
51. Takasaki H, Maruyama K, Takahashi F, Fujita M, Yoshida T, Nakashima K, Myouga F, Toyooka K, Yamaguchi-Shinozaki K, Shinozaki K (2015) SNAC-As, stress-responsive NAC transcription factors, mediate ABA-inducible leaf senescence. Plant J. doi:10.1111/tpj.13067
52. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
53. 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
54. Tran LS, 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
55. Van Moerkercke A, Steensma P, Schweizer F, Pollier J, Gariboldi I, Payne R, Vanden Bossche R, Miettinen K, Espoz J, Purnama PC, Kellner F, Seppänen-Laakso T, O’Connor SE, Rischer H, Memelink J, Goossens A (2015) The bHLH transcription factor BIS1 controls the iridoid branch of the monoterpenoid indole alkaloid pathway in Catharanthus roseus. Proc Natl Acad Sci USA 112:8130–8135
56. Weising K, Atkinson RG, Gardner RC (1995) Genomic fingerprinting by microsatellite-primed PCR: a critical evaluation. PCR Methods Appl 4:249–255
57. Wu A, Allu AD, Garapati P, Siddiqui H, Dortay H, Zanor MI, Asensi-Fabado MA, Munné-Bosch S, Antonio C, Tohge T, Fernie AR, Kaufmann K, Xue GP, Mueller-Roeber B, Balazadeh S (2012) JUNGBRUNNEN1, a reactive oxygen species–responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24:482–506
58. Xu B, Ohtani M, Yamaguchi M, Toyooka K, Wakazaki M, Sato M, Kubo M, Nakano Y, Sano R, Hiwatashi Y, Murata T, Kurata T, Yoneda A, Kato K, Hasebe M, Demura T (2014) Contribution of NAC transcription factors to plant adaptation to land. Science 343:1505–1508
59. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803
60. Yang YF, Wu J, Zhu K, Liu LQ, Chen FD, Yu DY (2009) Identification and characterization of two chrysanthemum (Dendronthema × moriforlium) DREB genes, belonging to the AP2/EREBP family. Mol Biol Rep 36:71–81
61. Yang Y, Ma C, Xu Y, Wei Q, Imtiaz M, Lan H, Gao S, Cheng L, Wang M, Fei Z, Hong B, Gao J (2014) A Zinc finger protein regulates flowering time and abiotic stress tolerance in chrysanthemum by modulating gibberellin biosynthesis. Plant cell 26:2038–2054
62. 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
63. Yokotani N, Tsuchida-Mayama T, Ichikawa H, Mitsuda N, Ohme-Takagi M, Kaku H, Minami E, Nishizawa Y (2014) OsNAC111, a blast disease–responsive transcription factor in rice, positively regulates the expression of defense-related genes. Mol Plant Microbe Interact 27:1027–1034
64. Yoo SY, Kim Y, Kim SY, Lee JS, Ahn JH (2007) Control of flowering time and cold response by a NAC-domain protein in Arabidopsis. PLoS One 25:e642
65. Yu X, Liu Y, Wang S, Tao Y, Wang Z, Shu Y, Peng H, Mijiti A, Wang Z, Zhang H, Ma H (2016) CarNAC4, a NAC-type chickpea transcription factor conferring enhanced drought and salt stress tolerances in Arabidopsis. Plant Cell Rep 35(3):613–627
66. Zhu JF, Li WF, Yang WH, Qi LW, Han SY (2013) Identification of microRNAs in by high-throughput sequencing and expression analysis and their targets under salt stress. Plant Cell Rep 32:1339–1349
67. Zhu M, Chen G, Zhang J, Zhang Y, Xie Q, Zhao Z, Pan Y, Hu Z (2014) 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