The HY5-PIF Regulatory Module Coordinates Light and Temperature Control of Photosynthetic Gene Transcription

PLoS Genetics

Volumn 10, Issue 6, 2014, Pages

  Toledo Ortiz, Gabriela ^a   Johansson, Henrik ^a,b   Lee, Keun Pyo ^a   Bou Torrent, Jordi ^c   Stewart, Kelly ^a   Steel, Gavin ^a   Rodríguez Concepción, Manuel ^c   Halliday, Karen J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; CHLOROPHYLL; PHYTOCHROME INTERACTING FACTOR PROTEIN; PHYTOENE SYNTHASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LONG HYPOCOTYL 5; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ARABIDOPSIS PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; G BOX BINDING FACTOR; HY5 PROTEIN, ARABIDOPSIS; NUCLEAR PROTEIN; PIF1 PROTEIN, ARABIDOPSIS; PSY1R PROTEIN, ARABIDOPSIS; RECEPTOR;

ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; ENVIRONMENTAL TEMPERATURE; GENE; GENE EXPRESSION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HY5 GENE; NONHUMAN; PHOTOSTIMULATION; PIFQ GENE; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; THERMOREGULATION; TRANSCRIPTION REGULATION; ARABIDOPSIS; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOTOPERIODICITY; PHOTOSYNTHESIS; SEASON; TEMPERATURE; TRANSCRIPTION INITIATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CAROTENOIDS; CHLOROPHYLL; G-BOX BINDING FACTORS; GENE EXPRESSION REGULATION, PLANT; NUCLEAR PROTEINS; PHOTOPERIOD; PHOTOSYNTHESIS; PROMOTER REGIONS, GENETIC; RECEPTORS, PEPTIDE; SEASONS; TEMPERATURE; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84903448591     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004416     Document Type: Article

References (81)

1. Leivar P, Quail PH, (2011) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16: 19-28.
2. Quail PH, (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3: 85-93.
3. Welsch R, Beyer P, Hugueney P, Kleinig H, von Lintig J, (2000) Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis. Planta 211: 846-854.
4. Tepperman JM, Hudson ME, Khanna R, Zhu T, Chang SH, et al. (2004) Expression profiling of phyB mutant demonstrates substantial contribution of other phytochromes to red-light-regulated gene expression during seedling de-etiolation. Plant J 38: 725-739.
5. Franklin KA, Quail PH, (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61: 11-24.
6. Reinbothe S, Reinbothe C, Apel K, Lebedev N, (1996) Evolution of chlorophyll biosynthesis-the challenge to survive photooxidation. Cell 86: 703-705.
7. Chen D, Xu G, Tang W, Jing Y, Ji Q, et al. (2013) Antagonistic basic helix-loop-helix/bZIP transcription factors form transcriptional modules that integrate light and reactive oxygen species signaling in Arabidopsis. Plant Cell 25: 1657-1673.
8. Huq E, Al-Sady B, Hudson M, Kim C, Apel K, et al. (2004) Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305: 1937-1941.
9. Niyogi KK, (1999) PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333-359.
10. Havaux M, Niyogi KK, (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci U S A 96: 8762-8767.
11. Walter MH, Strack D, (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28: 663-692.
12. Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL, (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9: R130.
13. Quail PH, (2010) Phytochromes. Curr Biol 20: R504-507.
14. Leivar P, Tepperman JM, Monte E, Calderon RH, Liu TL, et al. (2009) Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell 21: 3535-3553.
15. Shin J, Kim K, Kang H, Zulfugarov IS, Bae G, et al. (2009) Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochrome-interacting factors. Proc Natl Acad Sci U S A 106: 7660-7665.
16. Li J, Terzaghi W, Deng XW, (2012) Genomic basis for light control of plant development. Protein Cell 3: 106-116.
17. Toledo-Ortiz G, Huq E, Rodriguez-Concepcion M, (2010) Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc Natl Acad Sci U S A 107: 11626-11631.
18. Martinez-Garcia JF, Huq E, Quail PH, (2000) Direct targeting of light signals to a promoter element-bound transcription factor. Science 288: 859-863.
19. Shin J, Park E, Choi G, (2007) PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J 49: 981-994.
20. Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, et al. (2012) Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J 71: 699-711.
21. Zhang Y, Mayba O, Pfeiffer A, Shi H, Tepperman JM, et al. (2013) A quartet of PIF bHLH factors provides a transcriptionally centered signaling hub that regulates seedling morphogenesis through differential expression-patterning of shared target genes in Arabidopsis. PLoS Genet 9: e1003244.
22. Shen H, Moon J, Huq E, (2005) PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J 44: 1023-1035.
23. Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, et al. (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448: 358-361.
24. Soy J, Leivar P, Gonzalez-Schain N, Sentandreu M, Prat S, et al. (2012) Phytochrome-imposed oscillations in PIF3 protein abundance regulate hypocotyl growth under diurnal light/dark conditions in Arabidopsis. Plant J 71: 390-401.
25. Niwa Y, Yamashino T, Mizuno T, (2009) The circadian clock regulates the photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant Cell Physiol 50: 838-854.
26. Kunihiro A, Yamashino T, Nakamichi N, Niwa Y, Nakanishi H, et al. (2011) Phytochrome-interacting factor 4 and 5 (PIF4 and PIF5) activate the homeobox ATHB2 and auxin-inducible IAA29 genes in the coincidence mechanism underlying photoperiodic control of plant growth of Arabidopsis thaliana. Plant Cell Physiol 52: 1315-1329.
27. Nomoto Y, Kubozono S, Yamashino T, Nakamichi N, Mizuno T, (2012) Circadian clock- and PIF4-controlled plant growth: a coincidence mechanism directly integrates a hormone signaling network into the photoperiodic control of plant architectures in Arabidopsis thaliana. Plant Cell Physiol 53: 1950-1964.
28. Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, et al. (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19: 408-413.
29. Stavang JA, Gallego-Bartolome J, Gomez MD, Yoshida S, Asami T, et al. (2009) Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J 60: 589-601.
30. Foreman J, Johansson H, Hornitschek P, Josse EM, Fankhauser C, et al. (2011) Light receptor action is critical for maintaining plant biomass at warm ambient temperatures. Plant J 65: 441-452.
31. Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, et al. (2011) Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci U S A 108: 20231-20235.
32. Kumar SV, Lucyshyn D, Jaeger KE, Alos E, Alvey E, et al. (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484: 242-245.
33. Kami C, Lorrain S, Hornitschek P, Fankhauser C, (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91: 29-66.
34. Lau OS, Deng XW, (2010) Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol 13: 571-577.
35. Lee J, He K, Stolc V, Lee H, Figueroa P, et al. (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19: 731-749.
36. Oyama T, Shimura Y, Okada K, (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11: 2983-2995.
37. Zhang H, He H, Wang X, Wang X, Yang X, et al. (2011) Genome-wide mapping of the HY5-mediated gene networks in Arabidopsis that involve both transcriptional and post-transcriptional regulation. Plant J 65: 346-358.
38. Chattopadhyay S, Ang LH, Puente P, Deng XW, Wei N, (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10: 673-683.
39. Osterlund MT, Hardtke CS, Wei N, Deng XW, (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462-466.
40. Hardtke CS, Gohda K, Osterlund MT, Oyama T, Okada K, et al. (2000) HY5 stability and activity in arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J 19: 4997-5006.
41. Pokhilko A, Ramos JA, Holtan H, Maszle DR, Khanna R, et al. (2011) Ubiquitin ligase switch in plant photomorphogenesis: A hypothesis. J Theor Biol 270: 31-41.
42. Shin J, Anwer MU, Davis SJ, (2013) Phytochrome-interacting factors (PIFs) as bridges between environmental signals and the circadian clock: diurnal regulation of growth and development. Mol Plant 6: 592-595.
43. Catala R, Medina J, Salinas J, (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc Natl Acad Sci U S A 108: 16475-16480.
44. Zhang Y, Zheng S, Liu Z, Wang L, Bi Y, (2011) Both HY5 and HYH are necessary regulators for low temperature-induced anthocyanin accumulation in Arabidopsis seedlings. J Plant Physiol 168: 367-374.
45. Zhang Y, Liu Z, Liu R, Hao H, Bi Y, (2011) Gibberellins negatively regulate low temperature-induced anthocyanin accumulation in a HY5/HYH-dependent manner. Plant Signal Behav 6: 632-634.
46. Alabadi D, Blazquez MA, (2008) Integration of light and hormone signals. Plant Signal Behav 3: 448-449.
47. Nomoto Y, Kubozono S, Miyachi M, Yamashino T, Nakamichi N, 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: 1965-1973.
48. Toh S, McCourt P, Tsuchiya Y, (2012) HY5 is involved in strigolactone-dependent seed germination in Arabidopsis. Plant Signal Behav 7: 556-558.
49. Sun J, Qi L, Li Y, Chu J, Li C, (2012) PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating arabidopsis hypocotyl growth. PLoS Genet 8: e1002594.
50. Nomoto Y, Kubozono S, Miyachi M, Yamashino T, Nakamichi N,et al. (2012) Circadian clock and PIF4-mediated external coincidence mechanism coordinately integrates both of the cues from seasonal changes in photoperiod and temperature to regulate plant growth in Arabidopsis thaliana. Plant Signal Behav 8, 2, e22863.
51. Stephenson PG, Fankhauser C, Terry MJ, (2009) PIF3 is a repressor of chloroplast development. Proc Natl Acad Sci U S A 106: 7654-7659.
52. Rockholm DC, Yamamoto HY, (1996) Violaxanthin de-epoxidase. Plant Physiol 110: 697-703.
53. Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J, (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci U S A 98: 2053-2058.
54. Mochizuki N, Tanaka R, Grimm B, Masuda T, Moulin M, et al. (2010) The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci 15: 488-498.
55. Ben-Shem A, Frolow F, Nelson N, (2003) Crystal structure of plant photosystem I. Nature. 426: 630-635.
56. Alboresi A, Ballottari M, Hienerwadel R, Giacometti GM, Morosinotto T, (2009) Antenna complexes protect Photosystem I from photoinhibition. BMC Plant Biol 9: 71.
57. Franklin KA, Whitelam GC, (2005) Phytochromes and shade-avoidance responses in plants. Ann Bot 96: 169-175.
58. Moon J, Zhu L, Shen H, Huq E, (2008) PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. Proc Natl Acad Sci U S A 105: 9433-9438.
59. Kobayashi K, Obayashi T, Masuda T, (2012) Role of the G-box element in regulation of chlorophyll biosynthesis in Arabidopsis roots. Plant Signal Behav 7: 922-926.
60. Park E, Park J, Kim J, Nagatani A, Lagarias JC, et al. (2012) Phytochrome B inhibits binding of phytochrome-interacting factors to their target promoters. Plant J 72: 537-546.
61. Leivar P, Monte E, Cohn MM, Quail PH, (2012) Phytochrome signaling in green Arabidopsis seedlings: impact assessment of a mutually negative phyB-PIF feedback loop. Mol Plant 5: 734-749.
62. Al-Sady B, Ni W, Kircher S, Schafer E, Quail PH, (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol Cell 23: 439-446.
63. de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, et al. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480-484.
64. Henriques R, Jang IC, Chua NH, (2009) Regulated proteolysis in light-related signaling pathways. Curr Opin Plant Biol 12: 49-56.
65. Andronis C, Barak S, Knowles SM, Sugano S, Tobin EM, (2008) The clock protein CCA1 and the bZIP transcription factor HY5 physically interact to regulate gene expression in Arabidopsis. Mol Plant 1: 58-67.
66. Ito S, Matsushika A, Yamada H, Sato S, Kato T, et al. (2003) Characterization of the APRR9 pseudo-response regulator belonging to the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol 44: 1237-1245.
67. Makino S, Matsushika A, Kojima M, Yamashino T, Mizuno T, (2002) The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana: I. Characterization with APRR1-overexpressing plants. Plant Cell Physiol 43: 58-69.
68. Legnaioli T, Cuevas J, Mas P, (2009) TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J 28: 3745-3757.
69. Yamashino T, Matsushika A, Fujimori T, Sato S, Kato T, et al. (2003) A Link between circadian-controlled bHLH factors and the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol 44: 619-629.
70. Huang W, Perez-Garcia P, Pokhilko A, Millar AJ, Antoshechkin I, et al. (2012) Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336: 75-79.
71. Fukushima A, Kusano M, Nakamichi N, Kobayashi M, Hayashi N, et al. (2009) Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proc Natl Acad Sci U S A 106: 7251-7256.
72. Shen H, Zhu L, Castillon A, Majee M, Downie B, et al. (2008) Light-induced phosphorylation and degradation of the negative regulator PHYTOCHROME-INTERACTING FACTOR1 from Arabidopsis depend upon its direct physical interactions with photoactivated phytochromes. Plant Cell 20: 1586-1602.
73. Pokhilko A, Fernandez AP, Edwards KD, Southern MM, Halliday KJ, et al. (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol Syst Biol 8: 574.
74. Proveniers MC, van Zanten M, (2013) High temperature acclimation through PIF4 signaling. Trends Plant Sci 18: 59-64.
75. Lopez-Juez E, Dillon E, Magyar Z, Khan S, Hazeldine S, et al. (2008) Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell 20: 947-968.
76. del Pozo JC, Boniotti MB, Gutierrez C, (2002) Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light. Plant Cell 14: 3057-3071.
77. Berckmans B, Lammens T, Van Den Daele H, Magyar Z, Bogre L, et al. (2011) Light-dependent regulation of DEL1 is determined by the antagonistic action of E2Fb and E2Fc. Plant Physiol 157: 1440-1451.
78. Leivar P, Monte E, Oka Y, Liu T, Carle C, et al. (2008) Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr Biol 18: 1815-1823.
79. Hornitschek P, Lorrain S, Zoete V, Michielin O, Fankhauser C, (2009) Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J 28: 3893-3902.
80. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C, (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53: 312-323.
81. Yamashino T, Nomoto Y, Lorrain S, Miyachi M, Ito S, et al. (2013) Verification at the protein level of the PIF4-mediated external coincidence model for the temperature-adaptive photoperiodic control of plant growth in Arabidopsis thaliana. Plant Signal Behav 8: e23390.