Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis

Plant Physiology

Volumn 171, Issue 4, 2016, Pages 2744-2759

  Zhao, Chunzhao ^a,b   Zhang, Zhengjing ^a   Xie, Shaojun ^a,b   Si, Tong ^b,c   Li, Yuanya ^b,d   Zhu, Jian Kang ^a,b  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^b PURDUE UNIVERSITY   (United States)

^c NANJING AGRICULTURAL UNIVERSITY   (China)

^d YUNNAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; SODIUM CHLORIDE; TRANSCRIPTION FACTOR;

ACCLIMATIZATION; ARABIDOPSIS; COLD; DRUG EFFECTS; FREEZING; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; OSMOTIC PRESSURE; PHENOTYPE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENE; PLANT SEED;

ACCLIMATIZATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; COLD TEMPERATURE; FREEZING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GERMINATION; MUTATION; OSMOTIC PRESSURE; PHENOTYPE; SEEDS; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84982950029     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00533     Document Type: Article

References (54)

1. Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20: 2117–2129
2. Alonso-Blanco C, Gomez-Mena C, Llorente F, Koornneef M, Salinas J, Martínez-Zapater JM (2005) Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis. Plant Physiol 139: 1304–1312
3. Bailey TL, Machanick P (2012) Inferring direct DNA binding from ChIPseq. Nucleic Acids Res 40: e128
4. Carvallo MA, Pino MT, Jeknic Z, Zou C, Doherty CJ, Shiu SH, Chen TH, Thomashow MF (2011) A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana. J Exp Bot 62: 3807–3819
5. Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17: 1043–1054
6. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12: 444–451
7. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101: 15243–15248
8. Dong CH, Hu X, Tang W, Zheng X, Kim YS, Lee BH, Zhu JK (2006) A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Mol Cell Biol 26: 9533–9543
9. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38: W64-70
10. Gaj T, Gersbach CA, Barbas III CF (2013) ZFN, TALEN, and CRISPR/Casbased methods for genome engineering. Trends Biotechnol 31: 397–405
11. Gehan MA, Park S, Gilmour SJ, An C, Lee CM, Thomashow MF (2015) Natural variation in the C-repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes. Plant J 84: 682–693
12. Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54: 767–781
13. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124: 1854–1865
14. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in coldinduced COR gene expression. Plant J 16: 433–442
15. Gong Z, Lee H, Xiong L, Jagendorf A, Stevenson B, Zhu JK (2002) RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proc Natl Acad Sci USA 99: 11507–11512
16. Guan Q, Wu J, Zhang Y, Jiang C, Liu R, Chai C, Zhu J (2013) A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell 25: 342–356
17. Guo Y, Xiong L, Ishitani M, Zhu JK (2002) An Arabidopsis mutation in translation elongation factor 2 causes superinduction of CBF/DREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures. Proc Natl Acad Sci USA 99: 7786–7791
18. Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132: 220–235
19. Guy CL (1990) Cold acclimation and freezing stress tolerance: Role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41: 187–223
20. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110–2113
21. Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 1: e26
22. Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT (2002) Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 129: 1086–1094
23. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280: 104–106
24. Kim YS, Lee M, Lee JH, Lee HJ, Park CM (2015) The unified ICE-CBF pathway provides a transcriptional feedback control of freezing tolerance during cold acclimation in Arabidopsis. Plant Mol Biol 89: 187–201
25. Knight MR, Knight H (2012) Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 195: 737–751
26. Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17: 3155–3175
27. 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
28. Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D, et al (2015) COLD1 confers chilling tolerance in rice. Cell 160: 1209–1221
29. Mao Y, Zhang H, Xu N, Zhang B, Gou F, Zhu JK (2013) Application of the CRISPR-Cas system for efficient genome engineering in plants. Mol Plant 6: 2008–2011
30. Maruyama K, Takeda M, Kidokoro S, Yamada K, Sakuma Y, Urano K, Fujita M, Yoshiwara K, Matsukura S, Morishita Y, et al (2009) Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol 150: 1972–1980
31. McLeay RC, Bailey TL (2010) Motif Enrichment Analysis: a unified framework and an evaluation on ChIP data. BMC Bioinformatics 11: 165
32. Medina J, Bargues M, Terol J, Pérez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression Is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119: 463–470
33. Medina J, Catalá R, Salinas J (2011) The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci 180: 3–11
34. Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47: 541–568
35. Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101: 3985–3990
36. Novillo F, Medina J, Salinas J (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104: 21002–21007
37. Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138: 341–351
38. Park S, Lee CM, Doherty CJ, Gilmour SJ, Kim Y, Thomashow MF (2015) Regulation of the Arabidopsis CBF regulon by a complex low-temperature regulatory network. Plant J 82: 193–207
39. Popova AV, Rausch S, Hundertmark M, Gibon Y, Hincha DK (2015) The intrinsically disordered protein LEA7 from Arabidopsis thaliana protects the isolated enzyme lactate dehydrogenase and enzymes in a soluble leaf proteome during freezing and drying. Biochim Biophys Acta 1854 (10 Pt A): 1517–1525
40. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi- Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydrationand cold-inducible gene expression. Biochem Biophys Res Commun 290: 998–1009
41. Sasaki K, Christov NK, Tsuda S, Imai R (2014) Identification of a novel LEA protein involved in freezing tolerance in wheat. Plant Cell Physiol 55: 136–147
42. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a fulllength cDNA microarray. Plant Cell 13: 61–72
43. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, et al (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31: 279–292
44. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94: 1035–1040
45. Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi- Shinozaki K, Shinozaki K (2002) Important roles of drought- and coldinducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29: 417–426
46. Thalhammer A, Hincha DK (2014) A mechanistic model of COR15 protein function in plant freezing tolerance: integration of structural and functional characteristics. Plant Signal Behav 9: e977722
47. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50: 571–599
48. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562–578
49. Vergnolle C, Vaultier MN, Taconnat L, Renou JP, Kader JC, Zachowski A, Ruelland E (2005) The cold-induced early activation of phospholipase C and D pathways determines the response of two distinct clusters of genes in Arabidopsis cell suspensions. Plant Physiol 139: 1217–1233
50. Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41: 195–211
51. Wang Y, Hua J (2009) A moderate decrease in temperature induces COR15a expression through the CBF signaling cascade and enhances freezing tolerance. Plant J 60: 340–349
52. Zarka DG, Vogel JT, Cook D, Thomashow MF (2003) Cold induction of Arabidopsis CBF genes involves multiple ICE (inducer of CBF expression) promoter elements and a cold-regulatory circuit that is desensitized by low temperature. Plant Physiol 133: 910–918
53. Zhang Z, Mao Y, Ha S, Liu W, Botella JR, Zhu JK (2015) A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis. Plant Cell Rep 35: 1519–1533
54. Zhao C, Lang Z, Zhu JK (2015) Cold responsive gene transcription becomes more complex. Trends Plant Sci 20: 466–468