Hsfb2b-mediated repression of PRR7 directs abiotic stress responses of the circadian clock

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 45, 2014, Pages 16172-16177

  Kolmos, Elsebeth ^a   Chow, Brenda Y ^a   Pruneda Paz, Jose L ^b   Kay, Steve A ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

Author keywords

Circadian clock; Heat compensation; Hsf; Salt tolerance

Indexed keywords

HEAT SHOCK FACTOR B2B PROTEIN; PROTEIN; PRR7 PROTEIN; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; DNA BINDING PROTEIN; HEAT SHOCK PROTEIN; HEAT STRESS TRANSCRIPTION FACTORS; HSFB2B PROTEIN, ARABIDOPSIS; PRR7 PROTEIN, ARABIDOPSIS; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ABIOTIC STRESS; ARTICLE; BIOLUMINESCENCE; CIRCADIAN RHYTHM; CONTROLLED STUDY; FLOWERING; GENE INSERTION; HEAT STRESS; LOSS OF FUNCTION MUTATION; MOLECULAR CLONING; NONHUMAN; PLANT GROWTH; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALT STRESS; THERMAL EXPOSURE; ARABIDOPSIS; BIOSYNTHESIS; FLOWER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CIRCADIAN CLOCKS; DNA-BINDING PROTEINS; FLOWERS; GENE EXPRESSION REGULATION, PLANT; HEAT-SHOCK PROTEINS; HYPOCOTYL; PLANT PROTEINS; REPRESSOR PROTEINS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84909595110     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1418483111     Document Type: Article

References (66)

1. Rensing L, Ruoff P (2002) Temperature effect on entrainment, phase shifting, and amplitude of circadian clocks and its molecular bases. Chronobiol Int 19(5):807-864.
2. Nagel DH, Kay SA (2012) Complexity in the wiring and regulation of plant circadian networks. Curr Biol 22(16):R648-R657.
3. Farré EM, Harmer SL, Harmon FG, Yanovsky MJ, Kay SA (2005) Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr Biol 15(1):47-54.
4. Nakamichi N, et al. (2010) PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22(3):594-605.
5. Makino S, Matsushika A, Kojima M, Oda Y, Mizuno T (2001) Light response of the circadian waves of the APRR1/TOC1 quintet: When does the quintet start singing rhythmically in Arabidopsis? Plant Cell Physiol 42(3):334-339.
6. Michael TP, et al. (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302(5647):1049-1053.
7. Eriksson ME, Hanano S, Southern MM, Hall A, Millar AJ (2003) Response regulator homologues have complementary, light-dependent functions in the Arabidopsis circadian clock. Planta 218(1):159-162.
8. Yamamoto Y, et al. (2003) Comparative genetic studies on the APRR5 and APRR7 genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm, control of flowering time, and early photomorphogenesis. Plant Cell Physiol 44(11):1119-1130.
9. Salomé PA, McClung CR (2005) PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock. Plant Cell 17(3):791-803.
10. Salomé PA, Weigel D, McClung CR (2010) The role of the Arabidopsis morning loop components CCA1, LHY, PRR7, and PRR9 in temperature compensation. Plant Cell 22(11):3650-3661.
11. McClung CR, Davis SJ (2010) Ambient thermometers in plants: From physiological outputs towards mechanisms of thermal sensing. Curr Biol 20(24):R1086-R1092.
12. McWatters HG, Bastow RM, Hall A, Millar AJ (2000) The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408(6813):716-720.
13. Nagano AJ, et al. (2012) Deciphering and prediction of transcriptome dynamics under fluctuating field conditions. Cell 151(6):1358-1369.
14. Millar AJ, Kay SA (1996) Integration of circadian and phototransduction pathways in the network controlling CAB gene transcription in Arabidopsis. Proc Natl Acad Sci USA 93(26):15491-15496.
15. Nover L, et al. (2001) Arabidopsis and the heat stress transcription factor world: How many heat stress transcription factors do we need? Cell Stress Chaperones 6(3):177-189.
16. Scharf K-D, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: Structure, function and evolution. Biochim Biophys Acta 1819(2):104-119.
17. Von Koskull-Döring P, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12(10):452-457.
18. Franco-Zorrilla JM, et al. (2014) DNA-binding specificities of plant transcription factors and their potential to define target genes. Proc Natl Acad Sci USA 111(6):2367-2372.
19. Ikeda M, Ohme-Takagi M (2009) A novel group of transcriptional repressors in Arabidopsis. Plant Cell Physiol 50(5):970-975.
20. Zhu X, Thalor SK, Takahashi Y, Berberich T, Kusano T (2012) An inhibitory effect of the sequence-conserved upstream open-reading frame on the translation of the main open-reading frame of HsfB1 transcripts in Arabidopsis. Plant Cell Environ 35(11):2014-2030.
21. Busch W, Wunderlich M, Schöffl F (2005) Identification of novel heat shock factordependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41(1):1-14.
22. Ikeda M, Mitsuda N, Ohme-Takagi M (2011) Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol 157(3):1243-1254.
23. Pruneda-Paz JL, et al. (2014) A genome-scale resource for the functional characterization of Arabidopsis transcription factors. Cell Reports 8(2):622-632.
24. Bharti K, et al. (2004) Tomato heat stress transcription factor HsfB1 represents a novel type of general transcription coactivator with a histone-like motif interacting with the plant CREB-binding protein ortholog HAC1. Plant Cell 16(6):1521-1535.
25. Michael TP, et al. (2008) Network discovery pipeline elucidates conserved time-ofday-specific cis-regulatory modules. PLoS Genet 4(2):e14.
26. Kumar M, et al. (2009) Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. Mol Plant 2(1):152-165.
27. Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37(3):118-125.
28. Michael TP, Salomé PA, McClung CR (2003) Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proc Natl Acad Sci USA 100(11):6878-6883.
29. Thines B, Harmon FG (2010) Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock. Proc Natl Acad Sci USA 107(7):3257-3262.
30. Xiang J, et al. (2013) Heat shock factor OsHsfB2b negatively regulates drought and salt tolerance in rice. Plant Cell Rep 32(11):1795-1806.
31. Colmenero-Flores JM, Rosales MA (2014) Interaction between salt and heat stress: When two wrongs make a right. Plant Cell Environ 37(5):1042-1045.
32. Kim W-Y, et al. (2013) Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat Commun 4(1352):1352.
33. Farré EM, Kay SA (2007) PRR7 protein levels are regulated by light and the circadian clock in Arabidopsis. Plant J 52(3):548-560.
34. Liu T, Carlsson J, Takeuchi T, Newton L, Farré EM (2013) Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant J 76(1):101-114.
35. Nozue K, et al. (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448(7151):358-361.
36. Nusinow DA, et al. (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475(7356):398-402.
37. Ang LH, et al. (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1(2):213-222.
38. Jiang L, et al. (2012) Arabidopsis STO/BBX24 negatively regulates UV-B signaling by interacting with COP1 and repressing HY5 transcriptional activity. Cell Res 22(6):1046-1057.
39. Gangappa SN, Botto JF (2014) The BBX family of plant transcription factors. Trends Plant Sci 19(7):460-470.
40. Zhang X, et al. (2007) Constitutive expression of CIR1 (RVE2) affects several circadianregulated processes and seed germination in Arabidopsis. Plant J 51(3):512-525.
41. Kuno N, et al. (2003) The novel MYB protein EARLY-PHYTOCHROME-RESPONSIVE1 is a component of a slave circadian oscillator in Arabidopsis. Plant Cell 15(10):2476-2488.
42. Gangappa SN, et al. (2013) The Arabidopsis B-BOX protein BBX25 interacts with HY5, negatively regulating BBX22 expression to suppress seedling photomorphogenesis. Plant Cell 25(4):1243-1257.
43. Mitsuda N, Umemura Y, Ikeda M, Shikata M (2008) FioreDB: A database of phenotypic information induced by the chimeric repressor silencing technology (CRES-T) in Arabidopsis and floricultural plants. Plant Biotechnol 25(1):37-41.
44. Buhr ED, Yoo S-H, Takahashi JS (2010) Temperature as a universal resetting cue for mammalian circadian oscillators. Science 330(6002):379-385.
45. Reinke H, et al. (2008) Differential display of DNA-binding proteins reveals heat-shock factor 1 as a circadian transcription factor. Genes Dev 22(3):331-345.
46. Nishizawa-Yokoi A, Yoshida E, Yabuta Y, Shigeoka S (2009) Analysis of the regulation of target genes by an Arabidopsis heat shock transcription factor, HsfA2. Biosci Biotechnol Biochem 73(4):890-895.
47. Schramm F, et al. (2006) The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol Biol 60(5):759-772.
48. Hwang JE, et al. (2012) Overexpression of Arabidopsis dehydration-responsive elementbinding protein 2C confers tolerance to oxidative stress. Mol Cells 33(2):135-140.
49. Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: Integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11(8):545-555.
50. Mendillo ML, et al. (2012) HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 150(3):549-562.
51. Yan J, Wang H, Liu Y, Shao C (2008) Analysis of gene regulatory networks in the mammalian circadian rhythm. PLOS Comput Biol 4(10):e1000193.
52. Winter D, et al. (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2(8):e718.
53. Kim T-S, et al. (2011) HSP90 functions in the circadian clock through stabilization of the client F-box protein ZEITLUPE. Proc Natl Acad Sci U S A 108(40):16843-16848.
54. Sangster TA, et al. (2007) Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS ONE 2(7):e648.
55. Wu H-J, et al. (2012) Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc Natl Acad Sci USA 109(30):12219-12224.
56. Kumar SV, et al. (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484(7393):242-245.
57. Nomoto Y, et al. (2012) A circadian clock- and PIF4-mediated double coincidence mechanism is implicated in the thermosensitive photoperiodic control of plant architectures in Arabidopsis thaliana. Plant Cell Physiol 53(11):1965-1973.
58. Nakamichi N, et al. (2012) Transcriptional repressor PRR5 directly regulates clockoutput pathways. Proc Natl Acad Sci USA 109(42):17123-17128.
59. De Lucas M, et al. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451(7177):480-484.
60. Toledo-Ortiz G, et al. (2014) The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLoS Genet 10(6):e1004416.
61. Pruneda-Paz JL, Breton G, Para A, Kay SA (2009) A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323(5920):1481-1485.
62. Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735-743.
63. Helfer A, et al. (2011) LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Curr Biol 21(2):126-133.
64. Gendron JM, et al. (2012) Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proc Natl Acad Sci USA 109(8):3167-3172.
65. Nakagawa T, Ishiguro S, Kimura T (2009) Gateway vectors for plant transformation. Plant Biotechnol 26(3):275-284.
66. Chow BY, et al. (2014) Transcriptional regulation of LUX by CBF1 mediates cold input to the circadian clock in Arabidopsis. Curr Biol 24(13):1518-1524.