The HY5-PIF Regulatory Module Coordinates Light and Temperature Control of Photosynthetic Gene Transcription
Plants, as sessile and photosynthetic organisms, have to constantly adjust their growth and development in response to the environment. While light and temperature are recognized as the most prominent environmental factors modulating plant photosynthetic metabolism, how the seasonal and daily adjustments are achieved is not understood. Global climate alterations will bring together the combination of light and temperature changes and will require an understanding of signal convergence. If we are to mitigate the impact of variable weather patterns on agriculture, it is critical to advance our understanding of the basis of plant responses to environmental variations. In our study we show that the antagonistic activity of key plant transcription factors involved in phytochrome red light photoreceptors signaling (PIFs and HY5) optimize photosynthetic pigment production in response to environmental cues. These light and temperature responsive transcription factors operate in cooperation with the circadian clock to regulate photosynthetic pigment production through a common gene promoter element.
Vyšlo v časopise:
The HY5-PIF Regulatory Module Coordinates Light and Temperature Control of Photosynthetic Gene Transcription. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004416
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004416
Souhrn
Plants, as sessile and photosynthetic organisms, have to constantly adjust their growth and development in response to the environment. While light and temperature are recognized as the most prominent environmental factors modulating plant photosynthetic metabolism, how the seasonal and daily adjustments are achieved is not understood. Global climate alterations will bring together the combination of light and temperature changes and will require an understanding of signal convergence. If we are to mitigate the impact of variable weather patterns on agriculture, it is critical to advance our understanding of the basis of plant responses to environmental variations. In our study we show that the antagonistic activity of key plant transcription factors involved in phytochrome red light photoreceptors signaling (PIFs and HY5) optimize photosynthetic pigment production in response to environmental cues. These light and temperature responsive transcription factors operate in cooperation with the circadian clock to regulate photosynthetic pigment production through a common gene promoter element.
Zdroje
1. LeivarP, QuailPH (2011) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16: 19–28.
2. QuailPH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3: 85–93.
3. WelschR, BeyerP, HugueneyP, KleinigH, von LintigJ (2000) Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis. Planta 211: 846–854.
4. TeppermanJM, HudsonME, KhannaR, ZhuT, ChangSH, 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. FranklinKA, QuailPH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61: 11–24.
6. ReinbotheS, ReinbotheC, ApelK, LebedevN (1996) Evolution of chlorophyll biosynthesis–the challenge to survive photooxidation. Cell 86: 703–705.
7. ChenD, XuG, TangW, JingY, JiQ, 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. HuqE, Al-SadyB, HudsonM, KimC, ApelK, et al. (2004) Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305: 1937–1941.
9. NiyogiKK (1999) PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333–359.
10. HavauxM, NiyogiKK (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. WalterMH, StrackD (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28: 663–692.
12. CovingtonMF, MaloofJN, StraumeM, KaySA, HarmerSL (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9: R130.
13. QuailPH (2010) Phytochromes. Curr Biol 20: R504–507.
14. LeivarP, TeppermanJM, MonteE, CalderonRH, LiuTL, 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. ShinJ, KimK, KangH, ZulfugarovIS, BaeG, 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. LiJ, TerzaghiW, DengXW (2012) Genomic basis for light control of plant development. Protein Cell 3: 106–116.
17. Toledo-OrtizG, HuqE, Rodriguez-ConcepcionM (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-GarciaJF, HuqE, QuailPH (2000) Direct targeting of light signals to a promoter element-bound transcription factor. Science 288: 859–863.
19. ShinJ, ParkE, ChoiG (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. HornitschekP, KohnenMV, LorrainS, RougemontJ, LjungK, 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. ZhangY, MaybaO, PfeifferA, ShiH, TeppermanJM, 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. ShenH, MoonJ, HuqE (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. NozueK, CovingtonMF, DuekPD, LorrainS, FankhauserC, et al. (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448: 358–361.
24. SoyJ, LeivarP, Gonzalez-SchainN, SentandreuM, PratS, 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. NiwaY, YamashinoT, MizunoT (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. KunihiroA, YamashinoT, NakamichiN, NiwaY, NakanishiH, 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. NomotoY, KubozonoS, YamashinoT, NakamichiN, MizunoT (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. KoiniMA, AlveyL, AllenT, TilleyCA, HarberdNP, et al. (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19: 408–413.
29. StavangJA, Gallego-BartolomeJ, GomezMD, YoshidaS, AsamiT, et al. (2009) Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J 60: 589–601.
30. ForemanJ, JohanssonH, HornitschekP, JosseEM, FankhauserC, et al. (2011) Light receptor action is critical for maintaining plant biomass at warm ambient temperatures. Plant J 65: 441–452.
31. FranklinKA, LeeSH, PatelD, KumarSV, SpartzAK, 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. KumarSV, LucyshynD, JaegerKE, AlosE, AlveyE, et al. (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484: 242–245.
33. KamiC, LorrainS, HornitschekP, FankhauserC (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91: 29–66.
34. LauOS, DengXW (2010) Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol 13: 571–577.
35. LeeJ, HeK, StolcV, LeeH, FigueroaP, 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. OyamaT, ShimuraY, OkadaK (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11: 2983–2995.
37. ZhangH, HeH, WangX, WangX, YangX, 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. ChattopadhyayS, AngLH, PuenteP, DengXW, WeiN (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10: 673–683.
39. OsterlundMT, HardtkeCS, WeiN, DengXW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462–466.
40. HardtkeCS, GohdaK, OsterlundMT, OyamaT, OkadaK, et al. (2000) HY5 stability and activity in arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J 19: 4997–5006.
41. PokhilkoA, RamosJA, HoltanH, MaszleDR, KhannaR, et al. (2011) Ubiquitin ligase switch in plant photomorphogenesis: A hypothesis. J Theor Biol 270: 31–41.
42. ShinJ, AnwerMU, DavisSJ (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. CatalaR, MedinaJ, SalinasJ (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. ZhangY, ZhengS, LiuZ, WangL, BiY (2011) Both HY5 and HYH are necessary regulators for low temperature-induced anthocyanin accumulation in Arabidopsis seedlings. J Plant Physiol 168: 367–374.
45. ZhangY, LiuZ, LiuR, HaoH, BiY (2011) Gibberellins negatively regulate low temperature-induced anthocyanin accumulation in a HY5/HYH-dependent manner. Plant Signal Behav 6: 632–634.
46. AlabadiD, BlazquezMA (2008) Integration of light and hormone signals. Plant Signal Behav 3: 448–449.
47. NomotoY, KubozonoS, MiyachiM, YamashinoT, NakamichiN, 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. TohS, McCourtP, TsuchiyaY (2012) HY5 is involved in strigolactone-dependent seed germination in Arabidopsis. Plant Signal Behav 7: 556–558.
49. SunJ, QiL, LiY, ChuJ, LiC (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. StephensonPG, FankhauserC, TerryMJ (2009) PIF3 is a repressor of chloroplast development. Proc Natl Acad Sci U S A 106: 7654–7659.
52. RockholmDC, YamamotoHY (1996) Violaxanthin de-epoxidase. Plant Physiol 110: 697–703.
53. MochizukiN, BrusslanJA, LarkinR, NagataniA, ChoryJ (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. MochizukiN, TanakaR, GrimmB, MasudaT, MoulinM, et al. (2010) The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci 15: 488–498.
55. Ben-ShemA, FrolowF, NelsonN (2003) Crystal structure of plant photosystem I. Nature. 426: 630–635.
56. AlboresiA, BallottariM, HienerwadelR, GiacomettiGM, MorosinottoT (2009) Antenna complexes protect Photosystem I from photoinhibition. BMC Plant Biol 9: 71.
57. FranklinKA, WhitelamGC (2005) Phytochromes and shade-avoidance responses in plants. Ann Bot 96: 169–175.
58. MoonJ, ZhuL, ShenH, HuqE (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. KobayashiK, ObayashiT, MasudaT (2012) Role of the G-box element in regulation of chlorophyll biosynthesis in Arabidopsis roots. Plant Signal Behav 7: 922–926.
60. ParkE, ParkJ, KimJ, NagataniA, LagariasJC, et al. (2012) Phytochrome B inhibits binding of phytochrome-interacting factors to their target promoters. Plant J 72: 537–546.
61. LeivarP, MonteE, CohnMM, QuailPH (2012) Phytochrome signaling in green Arabidopsis seedlings: impact assessment of a mutually negative phyB-PIF feedback loop. Mol Plant 5: 734–749.
62. Al-SadyB, NiW, KircherS, SchaferE, QuailPH (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol Cell 23: 439–446.
63. de LucasM, DaviereJM, Rodriguez-FalconM, PontinM, Iglesias-PedrazJM, et al. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480–484.
64. HenriquesR, JangIC, ChuaNH (2009) Regulated proteolysis in light-related signaling pathways. Curr Opin Plant Biol 12: 49–56.
65. AndronisC, BarakS, KnowlesSM, SuganoS, TobinEM (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. ItoS, MatsushikaA, YamadaH, SatoS, KatoT, 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. MakinoS, MatsushikaA, KojimaM, YamashinoT, MizunoT (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. LegnaioliT, CuevasJ, MasP (2009) TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J 28: 3745–3757.
69. YamashinoT, MatsushikaA, FujimoriT, SatoS, KatoT, 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. HuangW, Perez-GarciaP, PokhilkoA, MillarAJ, AntoshechkinI, et al. (2012) Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336: 75–79.
71. FukushimaA, KusanoM, NakamichiN, KobayashiM, HayashiN, 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. ShenH, ZhuL, CastillonA, MajeeM, DownieB, 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. PokhilkoA, FernandezAP, EdwardsKD, SouthernMM, HallidayKJ, et al. (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol Syst Biol 8: 574.
74. ProveniersMC, van ZantenM (2013) High temperature acclimation through PIF4 signaling. Trends Plant Sci 18: 59–64.
75. Lopez-JuezE, DillonE, MagyarZ, KhanS, HazeldineS, 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 PozoJC, BoniottiMB, GutierrezC (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. BerckmansB, LammensT, Van Den DaeleH, MagyarZ, BogreL, et al. (2011) Light-dependent regulation of DEL1 is determined by the antagonistic action of E2Fb and E2Fc. Plant Physiol 157: 1440–1451.
78. LeivarP, MonteE, OkaY, LiuT, CarleC, et al. (2008) Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr Biol 18: 1815–1823.
79. HornitschekP, LorrainS, ZoeteV, MichielinO, FankhauserC (2009) Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J 28: 3893–3902.
80. LorrainS, AllenT, DuekPD, WhitelamGC, FankhauserC (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53: 312–323.
81. YamashinoT, NomotoY, LorrainS, MiyachiM, ItoS, 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.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2014 Číslo 6
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