Isolation and characterization of six AP2/ERF transcription factor genes in Chrysanthemum nankingense

International Journal of Molecular Sciences

Volumn 16, Issue 1, 2015, Pages 2052-2065

  Gao, Chunyan ^a,b   Li, Peiling ^a   Song, Aiping ^a   Wang, Haibin ^a   Wang, Yinjie ^a   Ren, Liping ^a   Qi, Xiangyu ^a   Chen, Fadi ^a   Jiang, Jiafu ^a   Chen, Sumei ^a,b  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b Jiangsu Province Engineering Lab for Modern Facility Agriculture Technology and Equipment   (China)

Author keywords

Hormone; PCR; Stress response; Transcription pattern

Indexed keywords

ABSCISIC ACID; COMPLEMENTARY DNA; JASMONIC ACID; SALICYLIC ACID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP2; TRANSCRIPTION FACTOR ERF; UNCLASSIFIED DRUG; MESSENGER RNA; PEPTIDE; VEGETABLE PROTEIN;

ABIOTIC STRESS; ARTICLE; CELLULAR DISTRIBUTION; CHRYSANTHEMUM; CHRYSANTHEMUM NANKINGENSE; CONTROLLED STUDY; GENE; GENE EXPRESSION PROFILING; GENE ISOLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; TEMPERATURE STRESS; TRANSACTIVATION ASSAY; TRANSCRIPTION FACTOR AP2 GENE; TRANSCRIPTION FACTOR ERF GENE; TRANSCRIPTION REGULATION; TRANSIENT EXPRESSION; AMINO ACID SEQUENCE; ARABIDOPSIS; CELL FRACTIONATION; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; ONION; PHYSIOLOGICAL STRESS; PLANT EPIDERMIS; PLANT GENE; PROTEIN TRANSPORT; TRANSCRIPTION INITIATION;

CHRYSANTHEMUM NANKINGENSE;

AMINO ACID SEQUENCE; ARABIDOPSIS; CHRYSANTHEMUM; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MOLECULAR SEQUENCE DATA; ONIONS; PEPTIDES; PLANT EPIDERMIS; PLANT PROTEINS; PROTEIN TRANSPORT; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; SUBCELLULAR FRACTIONS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84921501184     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16012052     Document Type: Article

References (48)

1. Anderson, J.P.; Badruzsaufari, E.; Schenk, P.M.; Manners, J.M.; Desmond, O.J.; Ehlert, C.; Maclean, D.J.; Ebert, P.R.; Kazan, K. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 2004, 16, 3460-3479.
2. Ashraf, M. Inducing drought tolerance in plants: Recent advances. Biotechnol. Adv. 2010, 28, 169-183.
3. Okamuro, J.K.; Caster, B.; Villarroel, R.; van Montagu, M.; Jofuku, K.D. The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc. Natl. Acad. Sci. USA 1997, 94, 7076-7081.
4. Zhuang, J.; Cai, B.; Peng, R.; Zhu, B.; Jin, X.; Xue, Y.; Gao, F.; Fu, X.; Tian, Y.; Zhao, W. Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. Biochem. Biophys. Res. Commun. 2008, 371, 468-474.
5. Zhuang, J.; Peng, R.; Cheng, Z.M.; Zhang, J.; Cai, B.; Zhang, Z.; Gao, F.; Zhu, B.; Fu, X.; Jin, X. Genome-wide analysis of the putative AP2/ERF family genes in Vitis vinifera. Sci. Hortic. 2009, 123, 73-81.
6. Qin, Q.; Liu, J.; Zhang, Z.; Peng, R.; Xiong, A.; Yao, Q.; Chen, J. Isolation, optimization, and functional analysis of the cDNA encoding transcription factor OsDREB1B in Oryza Sativa L. Mol. Breed. 2007, 19, 329-340.
7. Boutilier, K.; Offringa, R.; Sharma, V.K.; Kieft, H.; Ouellet, T.; Zhang, L.; Hattori, J.; Liu, C.-M.; van Lammeren, A.A.; Miki, B.L. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 2002, 14, 1737-1749.
8. Alonso, J.M.; Stepanova, A.N.; Leisse, T.J.; Kim, C.J.; Chen, H.; Shinn, P.; Stevenson, D.K.; Zimmerman, J.; Barajas, P.; Cheuk, R. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003, 301, 653-657.
9. Sohn, K.H.; Lee, S.C.; Jung, H.W.; Hong, J.K.; Hwang, B.K. Expression and functional roles of the pepper pathogen-induced transcription factor RAV1 in bacterial disease resistance, and drought and salt stress tolerance. Plant Mol. Biol. 2006, 61, 897-915.
10. Thomashow, M.F. Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Biol. 1999, 50, 571-599.
11. Xu, Z.; Xia, L.; Chen, M.; Cheng, X.; Zhang, R.; Li, L.; Zhao, Y.; Lu, Y.; Ni, Z.; Liu, L. Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol. Biol. 2007, 65, 719-732.
12. Nakano, T.; Suzuki, K.; Fujimura, T.; Shinshi, H. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 2006, 140, 411-432.
13. Riaño-Pachón, D.M.; Ruzicic, S.; Dreyer, I.; Mueller-Roeber, B. PlnTFDB: An integrative plant transcription factor database. BMC Bioinform. 2007, 8, doi:10.1186/1471-2105-8-42.
14. Zhang, G.; Chen, M.; Chen, X.; Xu, Z.; Guan, S.; Li, L.; Li, A.; Guo, J.; Mao, L.; Ma, Y. Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J. Exp. Bot. 2008, 59, 4095-4107.
15. Zhuang, J.; Chen, J.; Yao, Q.; Xiong, F.; Sun, C.; Zhou, X.; Zhang, J.; Xiong, A. Discovery and expression profile analysis of AP2/ERF family genes from Triticum aestivum. Mol. Biol. Rep. 2011, 38, 745-753.
16. Zhao, H.; Liu, Z.; Hu, X.; Yin, J.; Li, W.; Rao, G.; Zhang, X.; Huang, C.; Anderson, N.; Zhang, Q. Chrysanthemum genetic resources and related genera of Chrysanthemum collected in China. Genet. Res. Crop. Evol. 2009, 56, 937-946.
17. Cheng, X.; Chen, S.; Chen, F.; Fang, W.; Deng, Y.; She, L. Interspecific hybrids between Dendranthema morifolium (Ramat.) Kitamura and D. nankingense (Nakai) Tzvel. achieved using ovary rescue and their cold tolerance characteristics. Euphytica 2010, 172, 101-108.
18. Gao, H.; Song, A.; Zhu, X.; Chen, F.; Jiang, J.; Chen, Y.; Sun, Y.; Shan, H.; Gu, C.; Li, P. The heterologous expression in Arabidopsis of a chrysanthemum Cys2/His2 zinc finger protein gene confers salinity and drought tolerance. Planta 2012, 235, 979-993.
19. Song, A.; An, J.; Guan, Z.; Jiang, J.; Chen, F.; Lou, W.; Fang, W.; Liu, Z.; Chen, S. The constitutive expression of a two transgene construct enhances the abiotic stress tolerance of chrysanthemum. Plant Physiol. Biochem. 2014, 80, 114-120.
20. Guo, A.; He, K.; Liu, D.; Bai, S.; Gu, X.; Wei, L.; Luo, J. DATF: A database of Arabidopsis transcription factors. Bioinformatics 2005, 21, 2568-2569.
21. Sakuma, Y.; Liu, Q.; Dubouzet, J.G.; Abe, H.; Shinozaki, K.; Yamaguchi-Shinozaki, K. DNA-Binding Specificity of the ERF/AP2 Domain of Arabidopsis DREBs, Transcription Factors Involved in Dehydration-and Cold-Inducible Gene Expression. Biochem. Biophys. Res. Commun. 2002, 290, 998-1009.
22. Khong, G.N.; Richaud, F.; Coudert, Y.; Pati, P.K.; Santi, C.; Périn, C.; Breitler, J.C.; Meynard, D.; Vinh, D.N.; Guiderdoni, E. Modulating rice stress tolerance by transcription factors. Biotechnol. Genet. Eng. 2008, 25, 381-404.
23. Hiratsu, K.; Matsui, K.; Koyama, T.; Ohme-Takagi, M. Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J. 2003, 34, 733-739.
24. Ohta, M.; Matsui, K.; Hiratsu, K.; Shinshi, H.; Ohme-Takagi, M., Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 2001, 13, 1959-1968.
25. Chen, M.; Wang, Q.-Y.; Cheng, X.-G.; Xu, Z.-S.; Li, L.-C.; Ye, X.-G.; Xia, L.-Q.; Ma, Y.-Z. GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem. Biophys. Res. Commun. 2007, 353, 299-305.
26. Sakuma, Y.; Maruyama, K.; Qin, F.; Osakabe, Y.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Nat. Acad. Sci. USA 2006, 103, 18822-18827.
27. Maruyama, K.; Sakuma, Y.; Kasuga, M.; Ito, Y.; Seki, M.; Goda, H.; Shimada, Y.; Yoshida, S.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J. 2004, 38, 982-993.
28. Tsutsui, T.; Kato, W.; Asada, Y.; Sako, K.; Sato, T.; Sonoda, Y.; Kidokoro, S.; Yamaguchi-Shinozaki, K.; Tamaoki, M.; Arakawa, K. DEAR1, a transcriptional repressor of DREB protein that mediates plant defense and freezing stress responses in Arabidopsis. J. Plant Res. 2009, 122, 633-643.
29. Dong, C.-J.; Liu, J.-Y. The Arabidopsis EAR-motif-containing protein RAP2.1 functions as an active transcriptional repressor to keep stress responses under tight control. BMC Plant Biol. 2010, 10, doi:10.1186/1471-2229-10-47.
30. Mizoi, J.; Shinozaki, K.; Yamaguchi-Shinozaki, K. AP2/ERF family transcription factors in plant abiotic stress responses. BBA Gene Regul. Mech. 2012, 1819, 86-96.
31. Tournier, B.; Sanchez-Ballesta, M.T.; Jones, B.; Pesquet, E.; Regad, F.; Latché, A.; Pech, J.; Bouzayen, M. New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element. FEBS Lett. 2003, 550, 149-154.
32. Fujimoto, S.Y.; Ohta, M.; Usui, A.; Shinshi, H.; Ohme-Takagi, M. Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 2000, 12, 393-404.
33. Fujita, M.; Fujita, Y.; Noutoshi, Y.; Takahashi, F.; Narusaka, Y.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 2006, 9, 436-442.
34. Yan, L.; Zhai, Q.; Wei, J.; Li, S.; Wang, B.; Huang, T.; Du, M.; Sun, J.; Kang, L.; Li, C. Role of Tomato Lipoxygenase D in Wound-Induced Jasmonate Biosynthesis and Plant Immunity to Insect Herbivores. PLoS Genet. 2013, 9, e1003964.
35. Cheng, M.; Liao, P.; Kuo, W.; Lin, T. The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol. 2013, 162, 1566-1582.
36. Kasuga, M.; Liu, Q.; Miura, S.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 1999, 17, 287-291.
37. Xu, Z.; Ni, Z.; Liu, L.; Nie, L.; Li, L.; Chen, M.; Ma, Y. Characterization of the TaAIDFa gene encoding a CRT/DRE-binding factor responsive to drought, high-salt, and cold stress in wheat. Mol. Genet. Genomics 2008, 280, 497-508.
38. Moran, P.J.; Thompson, G.A. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 2001, 125, 1074-1085.
39. Wang, H.; Jiang, J.; Chen, S.; Qi, X.; Peng, H.; Li, P.; Song, A.; Guan, Z.; Fang, W.; Liao, Y. Next-generation sequencing of the Chrysanthemum nankingense (Asteraceae) transcriptome permits large-scale unigene assembly and SSR marker discovery. PLoS One 2013, 8, e62293.
40. Larkin, M.; Blackshields, G.; Brown, N.; Chenna, R.; McGettigan, P.A.; McWilliam, H.; Valentin, F.; Wallace, I.M.; Wilm, A.; Lopez, R. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23, 2947-2948.
41. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731-2739.
42. Song, A.; Zhu, X.; Chen, F.; Gao, H.; Jiang, J.; Chen, S. A chrysanthemum heat shock protein confers tolerance to abiotic stress. Int. J. Mol. Sci. 2014, 15, 5063-5078.
43. + antiporter. Plant Biol. 2012, 14, 706-713.
44. Chen, Y.; Jiang, J.; Song, A.; Chen, S.; Shan, H.; Luo, H.; Gu, C.; Sun, J.; Zhu, L.; Fang, W.; Chen, F. Ambient temperature enhanced freezing tolerance of Chrysanthemum dichrum CdICE1 Arabidopsis via miR398. BMC Biol. 2013, 11, doi:10.1186/1741-7007-11-121.
45. Song, A.; Li, P.; Jiang, J.; Chen, S.; Li, H.; Zeng, J.; Shao, Y.; Zhu, L.; Zhang, Z.; Chen, F. Phylogenetic and transcription analysis of chrysanthemum WRKY transcription factors. Int. J. Mol. Sci. 2014, 15, 14442-14455.
46. -ΔΔCt Method. Methods 2001, 25, 402-408.
47. de Hoon, M.J.; Imoto, S.; Nolan, J.; Miyano, S. Open source clustering software. Bioinformatics 2004, 20, 1453-1454.
48. Eisen, M.B.; Spellman, P.T.; Brown, P.O.; Botstein, D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 1998, 95, 14863-14868.