Cold stress signaling networks in Arabidopsis

Journal of Plant Biology

Volumn 56, Issue 2, 2013, Pages 69-76

  Jeon, Jin ^a   Kim, Jungmook ^a  

^a Chonnam National University   (South Korea)

Author keywords

Circadian clock; Cold stress signaling; Crosstalk; Flowering; Phytohormone

Indexed keywords

EID: 84876121138     PISSN: 12269239     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12374-013-0903-y     Document Type: Review

References (70)

1. Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311: 91-94.
2. 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.
3. Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281: 37636-37645.
4. Ausin I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez-Zapater JM (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36: 162-166.
5. Bieniawska Z, Espinoza C, Schlereth A, Sulpice R, Hincha DK, Hannah MA (2008) Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the coldresponsive transcriptome. Plant Physiol 147: 263-279.
6. Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan BB, Gruissem W, Jones RL, eds. Biochemistry and molecular biology of plants. Rockville, MD: American Society of Plant Biologists, 1158-1203.
7. Carpaneto A, Ivashikina N, Levchenko V, Krol E, Jeworutzki E, Zhu JK, Hedrich R (2007) Cold transiently activates calciumpermeable channels in Arabidopsis mesophyll cells. Plant Physiol 143: 487-494.
8. 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.
9. Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55: 225-236.
10. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12: 444-451.
11. Deal RB, Topp CN, McKinney EC, Meagher RB (2007) Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A. Z. Plant Cell 19: 74-83.
12. Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309: 630-633.
13. Doherty CJ, van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in coldregulated gene expression and freezing tolerance. Plant Cell 21: 972-984.
14. Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci USA 103: 8281-8286.
15. Dong MA, Farre EM, Thomashow MF (2011) Circadian clockassociated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc Natl Acad Sci USA 108: 7241-7246.
16. Finkler A, Ashery-Padan R, Fromm H (2007) CAMTAs: calmodulinbinding transcription activators from plants to human. FEBS Lett 581: 3893-3898.
17. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14: 1675-1690.
18. Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137: 961-968.
19. 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 cold-induced COR gene expression. Plant J 16: 433-442.
20. 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.
21. Jeon J, Kim J (2011) FVE, an Arabidopsis homologue of the retinoblastoma-associated protein that regulates flowering time and cold response, binds to chromatin as a large multiprotein complex. Mol Cells 32: 227-234.
22. Jeon J, Kim J (2013) Arabidopsis Response Regulator1 and Arabidopsis Histidine Phosphotransfer Protein2 (AHP2), AHP3, and AHP5 function in cold signaling. Plant Physiol 161: 408-424.
23. Jeon J, Kim NY, Kim S, Kang NY, Novak O, Ku SJ, Cho C, Lee DJ, Lee EJ, Strnad M, Kim J (2010) A subset of cytokinin twocomponent signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem 285: 23371-23386.
24. Jung JH, Seo PJ, Park CM (2012) The E3 ubiquitin ligase HOS1 regulates Arabidopsis flowering by mediating CONSTANS degradation under cold stress. J Biol Chem 287: 43277-43287.
25. Kang NY, Cho C, Kim NY, Kim J (2012) Cytokinin receptordependent and receptor-independent pathways in the dehydration response of Arabidopsis thaliana. J Plant Physiol 169: 1382-1391.
26. Karashima Y, Talavera K, Everaerts W, Janssens A, Kwan KY, Vennekens R, Nilius B, Voets T (2009) TRPA1 acts as a cold sensor in vitro and in vivo. Proc Natl Acad Sci USA106: 1273-1278.
27. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17: 287-291.
28. Kim HJ, Hyun Y, Park JY, Park MJ, Park MK, Kim MD, Lee MH, Moon J, Lee I, Kim J (2004) A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat Genet 36: 167-171.
29. Kim J (2007) Perception, transduction, and networks in cold signaling. J Plant Biol 50: 139-147.
30. Kim J, Jeon J (2013) Cold signaling via the two-component signaling system. Mol Plant 6: 15-17.
31. Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8: 489-503.
32. Kumar SV, Wigge PA (2010) H2A. Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140: 136-147.
33. Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK (2001) The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Genes Dev 15: 912-924.
34. 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 lowtemperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10: 1391-1406.
35. Los DA, Ray MK, Murata N (1997) Differences in the control of the temperature-dependent expression of four genes for desaturases in Synechocystis sp. PCC 6803. Mol Microbiol 25: 1167-1175.
36. Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38: 982-993.
37. Mikami K, Kanesaki Y, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp PCC 6803. Mol Microbiol 46: 905-915.
38. Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19: 1403-1414.
39. Miura K, Ohta M, Nakazawa M, Ono M, Hasegawa PM (2011) ICE1 Ser403 is necessary for protein stabilization and regulation of cold signaling and tolerance. Plant J 67: 269-279.
40. Monroy AF, Sarhan F, Dhindsa RS (1993) Cold-induced changes in freezing tolerance, protein phosphorylation, and gene expression (Evidence for a role of calcium). Plant Physiol 102: 1227-1235.
41. Murata N, Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115: 875-879.
42. Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, Saito K, Sakakibara H, Mizuno T (2009) Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol 50: 447-462.
43. Orvar BL, Sangwan V, Omann F, Dhindsa RS (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 23: 785-794.
44. Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282: 10036-10046.
45. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002) A TRP channel that senses cold stimuli and menthol. Cell 108: 705-715.
46. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105-2110.
47. Rikin A, Dillwith JW, Bergman DK (1993) Correlation between the circadian rhythm of resistance to extreme temperatures and changes in fatty acid composition in cotton seedlings. Plant Physiol 101: 31-36.
48. Plieth C, Hansen UP, Knight H, Knight MR (1999) Temperature sensing by plants: the primary characteristics of signal perception and calcium response. Plant J 18: 491-497.
49. Sakai A, Larcher W (1987) Frost survival of plants: Responses and adaptation to freezing stress. Springer, Berlin.
50. 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.
51. Seo PJ, Kim MJ, Song JS, Kim YS, Kim HJ, Park CM (2010) Proteolytic processing of an Arabidopsis membrane-bound NAC transcription factor is triggered by cold-induced changes in membrane fluidity. Biochem J 427: 359-367.
52. Seo E, Lee H, Jeon J, Park H, Kim J, Noh YS, Lee I (2009) Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell 21: 3185-3197.
53. Seo PJ, Park MJ, Lim MH, Kim SG, Lee M, Baldwin IT, Park CM (2012) A self-regulatory circuit of CIRCADIAN CLOCKASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell 24: 2427-2442.
54. Shibasaki K, Uemura M, Tsurumi S, Rahman A (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell 21: 3823-3838.
55. 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.
56. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6: 410-417.
57. Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc Natl Acad Sci USA 95: 14570-14575.
58. 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.
59. Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40: 235-244.
60. Suzuki I, Los DA, Kanesaki Y, Mikami K, Murata N (2000) The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J 19: 1327-1334.
61. Tahtiharju S, Sangwan V, Monroy AF, Dhindsa RS, Borg M (1997) The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium. Planta 203: 442-447.
62. Thomashow MF (1999) PLANT COLD ACCLIMATION: Freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50: 571-599.
63. Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104: 20623-20628.
64. 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.
65. Whalley HJ, Sargeant AW, Steele JF, Lacoere T, Lamb R, Saunders NJ, Knight H, Knight MR (2011) Transcriptomic analysis reveals calcium regulation of specific promoter motifs in Arabidopsis. Plant Cell 23: 4079-4095.
66. Xin Z, Browse J (1998) Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc Natl Acad Sci USA 95: 7799-7804.
67. Xin Z, Mandaokar A, Chen J, Last RL, Browse J (2007) Arabidopsis ESK1 encodes a novel regulator of freezing tolerance. Plant J 49: 786-799.
68. Yamazaki T, Kawamura Y, Minami A, Uemura M (2008) Calciumdependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20: 3389-3404.
69. 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 2: e642.
70. Zhu J, Shi H, Lee BH, Damsz B, Cheng S, Stirm V, Zhu JK, Hasegawa PM, Bressan RA (2004) An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proc Natl Acad Sci USA 101: 9873-9878.