UVR8-mediated inhibition of shade avoidance involves HFR1 stabilization in Arabidopsis


Autoři: Eleni Tavridou aff001;  Emanuel Schmid-Siegert aff003;  Christian Fankhauser aff004;  Roman Ulm aff001
Působiště autorů: Department of Botany and Plant Biology, Section of Biology, Faculty of Science, University of Geneva, CH, Geneva, Switzerland aff001;  Institute of Genetics and Genomics of Geneva (iGE3), University of Geneva, Geneva, Switzerland aff002;  SIB-Swiss Institute of Bioinformatics, University of Lausanne, CH, Lausanne, Switzerland aff003;  Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH, Lausanne, Switzerland aff004
Vyšlo v časopise: UVR8-mediated inhibition of shade avoidance involves HFR1 stabilization in Arabidopsis. PLoS Genet 16(5): e32767. doi:10.1371/journal.pgen.1008797
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008797

Souhrn

Sun-loving plants perceive the proximity of potential light-competing neighboring plants as a reduction in the red:far-red ratio (R:FR), which elicits a suite of responses called the “shade avoidance syndrome” (SAS). Changes in R:FR are primarily perceived by phytochrome B (phyB), whereas UV-B perceived by UV RESISTANCE LOCUS 8 (UVR8) elicits opposing responses to provide a counterbalance to SAS, including reduced shade-induced hypocotyl and petiole elongation. Here we show at the genome-wide level that UVR8 broadly suppresses shade-induced gene expression. A subset of this gene regulation is dependent on the UVR8-stabilized atypical bHLH transcription regulator LONG HYPOCOTYL IN FAR-RED 1 (HFR1), which functions in part redundantly with PHYTOCHROME INTERACTING FACTOR 3-LIKE 1 (PIL1). In parallel, UVR8 signaling decreases protein levels of the key positive regulators of SAS, namely the bHLH transcription factors PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and PIF5, in a COP1-dependent but HFR1-independent manner. We propose that UV-B antagonizes SAS via two mechanisms: degradation of PIF4 and PIF5, and HFR1- and PIL1-mediated inhibition of PIF4 and PIF5 function. This work highlights the importance of typical and atypical bHLH transcription regulators for the integration of light signals from different photoreceptors and provides further mechanistic insight into the crosstalk of UVR8 signaling and SAS.

Klíčová slova:

Gene expression – Hypocotyl – Marker genes – Regulator genes – Seedlings – Transcriptional control – Ultraviolet B – White light


Zdroje

1. Galvao VC, Fankhauser C. Sensing the light environment in plants: photoreceptors and early signaling steps. Curr Opin Neurobiol. 2015; 34: 46–53. doi: 10.1016/j.conb.2015.01.013 25638281

2. Demarsy E, Goldschmidt-Clermont M, Ulm R. Coping with 'dark sides of the sun' through photoreceptor signaling. Trends Plant Sci. 2018; 23: 260–271. doi: 10.1016/j.tplants.2017.11.007 29233601

3. Casal JJ. Shade avoidance. Arabidopsis Book. 2012; 10: e0157. doi: 10.1199/tab.0157 22582029

4. Fiorucci AS, Fankhauser C. Plant strategies for enhancing access to sunlight. Curr Biol. 2017; 27: R931–R40. doi: 10.1016/j.cub.2017.05.085 28898666

5. Ballare CL, Pierik R. The shade-avoidance syndrome: multiple signals and ecological consequences. Plant Cell Environ. 2017; 40: 2530–2543. doi: 10.1111/pce.12914 28102548

6. Casal JJ. Photoreceptor signaling networks in plant responses to shade. Annu Rev Plant Biol. 2013; 64: 403–427. doi: 10.1146/annurev-arplant-050312-120221 23373700

7. Fraser DP, Hayes S, Franklin KA. Photoreceptor crosstalk in shade avoidance. Curr Opin Plant Biol. 2016; 33: 1–7. doi: 10.1016/j.pbi.2016.03.008 27060719

8. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 2008; 53: 312–323. doi: 10.1111/j.1365-313X.2007.03341.x 18047474

9. Shen Y, Khanna R, Carle CM, Quail PH. Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiol. 2007; 145: 1043–1051. doi: 10.1104/pp.107.105601 17827270

10. Leivar P, Monte E. PIFs: systems integrators in plant development. Plant Cell. 2014; 26: 56–78. doi: 10.1105/tpc.113.120857 24481072

11. Hornitschek P, Lorrain S, Zoete V, Michielin O, Fankhauser C. Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J. 2009; 28: 3893–3902. doi: 10.1038/emboj.2009.306 19851283

12. Rizzini L, Favory JJ, Cloix C, Faggionato D, O'Hara A, Kaiserli E, et al. Perception of UV-B by the Arabidopsis UVR8 protein. Science. 2011; 332: 103–106. doi: 10.1126/science.1200660 21454788

13. Favory JJ, Stec A, Gruber H, Rizzini L, Oravecz A, Funk M, et al. Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J. 2009; 28: 591–601. doi: 10.1038/emboj.2009.4 19165148

14. Oravecz A, Baumann A, Mate Z, Brzezinska A, Molinier J, Oakeley EJ, et al. CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell. 2006; 18: 1975–1990. doi: 10.1105/tpc.105.040097 16829591

15. Lau OS, Deng XW. The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci. 2012; 17: 584–593. doi: 10.1016/j.tplants.2012.05.004 22705257

16. Hoecker U. The activities of the E3 ubiquitin ligase COP1/SPA, a key repressor in light signaling. Curr Opin Plant Biol. 2017; 37: 63–69. doi: 10.1016/j.pbi.2017.03.015 28433946

17. Podolec R, Ulm R. Photoreceptor-mediated regulation of the COP1/SPA E3 ubiquitin ligase. Curr Opin Plant Biol. 2018; 45: 18–25. doi: 10.1016/j.pbi.2018.04.018 29775763

18. Lau K, Podolec R, Chappuis R, Ulm R, Hothorn M. Plant photoreceptors and their signaling components compete for COP1 binding via VP peptide motifs. EMBO J. 2019: e102140. doi: 10.15252/embj.2019102140 31304983

19. Huang X, Ouyang X, Yang P, Lau OS, Chen L, Wei N, et al. Conversion from CUL4-based COP1-SPA E3 apparatus to UVR8-COP1-SPA complexes underlies a distinct biochemical function of COP1 under UV-B. Proc Natl Acad Sci USA. 2013; 110: 16669–16674. doi: 10.1073/pnas.1316622110 24067658

20. Ulm R, Baumann A, Oravecz A, Mate Z, Adam E, Oakeley EJ, et al. Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc Natl Acad Sci USA. 2004; 101: 1397–1402. doi: 10.1073/pnas.0308044100 14739338

21. Brown BA, Cloix C, Jiang GH, Kaiserli E, Herzyk P, Kliebenstein DJ, et al. A UV-B-specific signaling component orchestrates plant UV protection. Proc Natl Acad Sci USA. 2005; 102: 18225–18230. doi: 10.1073/pnas.0507187102 16330762

22. Gruber H, Heijde M, Heller W, Albert A, Seidlitz HK, Ulm R. Negative feedback regulation of UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. Proc Natl Acad Sci USA. 2010; 107: 20132–20137. doi: 10.1073/pnas.0914532107 21041653

23. Stracke R, Favory JJ, Gruber H, Bartelniewoehner L, Bartels S, Binkert M, et al. The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant Cell Environ. 2010; 33: 88–103. doi: 10.1111/j.1365-3040.2009.02061.x 19895401

24. Huang X, Ouyang X, Yang P, Lau OS, Li G, Li J, et al. Arabidopsis FHY3 and HY5 positively mediate induction of COP1 transcription in response to photomorphogenic UV-B light. Plant Cell. 2012; 24: 4590–4606. doi: 10.1105/tpc.112.103994 23150635

25. Binkert M, Kozma-Bognar L, Terecskei K, De Veylder L, Nagy F, Ulm R. UV-B-responsive association of the Arabidopsis bZIP transcription factor ELONGATED HYPOCOTYL5 with target genes, including its own promoter. Plant Cell. 2014; 26: 4200–4213. doi: 10.1105/tpc.114.130716 25351492

26. Brown BA, Jenkins GI. UV-B signaling pathways with different fluence-rate response profiles are distinguished in mature Arabidopsis leaf tissue by requirement for UVR8, HY5, and HYH. Plant Physiol. 2008; 146: 576–588. doi: 10.1104/pp.107.108456 18055587

27. Tavridou E, Pireyre M, Ulm R. Degradation of the transcription factors PIF4 and PIF5 under UV-B promotes UVR8-mediated hypocotyl growth inhibition in Arabidopsis. Plant J. 2020; 101: 507–517. doi: 10.1111/tpj.14556 31571300

28. Hayes S, Velanis CN, Jenkins GI, Franklin KA. UV-B detected by the UVR8 photoreceptor antagonizes auxin signaling and plant shade avoidance. Proc Natl Acad Sci USA. 2014; 111: 11894–11899. doi: 10.1073/pnas.1403052111 25071218

29. Liang T, Mei S, Shi C, Yang Y, Peng Y, Ma L, et al. UVR8 interacts with BES1 and BIM1 to regulate transcription and photomorphogenesis in Arabidopsis. Dev Cell. 2018; 44: 512–523 doi: 10.1016/j.devcel.2017.12.028 29398622

30. Yang Y, Liang T, Zhang L, Shao K, Gu X, Shang R, et al. UVR8 interacts with WRKY36 to regulate HY5 transcription and hypocotyl elongation in Arabidopsis. Nat Plants. 2018; 4: 98–107. doi: 10.1038/s41477-017-0099-0 29379156

31. Kliebenstein DJ, Lim JE, Landry LG, Last RL. Arabidopsis UVR8 regulates ultraviolet-B signal transduction and tolerance and contains sequence similarity to human regulator of chromatin condensation 1. Plant Physiol. 2002; 130: 234–243. doi: 10.1104/pp.005041 12226503

32. Sharma A, Sharma B, Hayes S, Kerner K, Hoecker U, Jenkins GI, et al. UVR8 disrupts stabilisation of PIF5 by COP1 to inhibit plant stem elongation in sunlight. Nat Commun. 2019; 10: 4417. doi: 10.1038/s41467-019-12369-1 31562307

33. Mazza CA, Ballare CL. Photoreceptors UVR8 and phytochrome B cooperate to optimize plant growth and defense in patchy canopies. New Phytol. 2015; 207: 4–9. doi: 10.1111/nph.13332 25659974

34. Vandenbussche F, Tilbrook K, Fierro AC, Marchal K, Poelman D, Van Der Straeten D, et al. Photoreceptor-mediated bending towards UV-B in Arabidopsis. Mol Plant. 2014; 7: 1041–1052. doi: 10.1093/mp/ssu039 24711292

35. Fraser DP, Sharma A, Fletcher T, Budge S, Moncrieff C, Dodd AN, et al. UV-B antagonises shade avoidance and increases levels of the flavonoid quercetin in coriander (Coriandrum sativum). Sci Rep. 2017; 7: 17758. doi: 10.1038/s41598-017-18073-8 29259256

36. Hayes S, Sharma A, Fraser DP, Trevisan M, Cragg-Barber CK, Tavridou E, et al. UV-B perceived by the UVR8 photoreceptor inhibits plant thermomorphogenesis. Curr Biol. 2017; 27: 120–127. doi: 10.1016/j.cub.2016.11.004 27989670

37. Lorrain S, Trevisan M, Pradervand S, Fankhauser C. Phytochrome interacting factors 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. Plant J. 2009; 60: 449–461. doi: 10.1111/j.1365-313X.2009.03971.x 19619162

38. Toledo-Ortiz G, Johansson H, Lee KP, Bou-Torrent J, Stewart K, Steel G, et al. The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLoS Genet. 2014; 10: e1004416. doi: 10.1371/journal.pgen.1004416 24922306

39. Gangappa SN, Kumar SV. DET1 and HY5 Control PIF4-Mediated Thermosensory Elongation Growth through Distinct Mechanisms. Cell Rep. 2017; 18: 344–351. doi: 10.1016/j.celrep.2016.12.046 28076780

40. de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, Lorrain S, et al. A molecular framework for light and gibberellin control of cell elongation. Nature. 2008; 451: 480–484. doi: 10.1038/nature06520 18216857

41. Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, et al. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature. 2008; 451: 475–479. doi: 10.1038/nature06448 18216856

42. Duek PD, Elmer MV, van Oosten VR, Fankhauser C. The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1. Curr Biol. 2004; 14: 2296–2301. doi: 10.1016/j.cub.2004.12.026 15620659

43. Jang IC, Yang JY, Seo HS, Chua NH. HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev. 2005; 19: 593–602. doi: 10.1101/gad.1247205 15741320

44. Yang J, Lin R, Sullivan J, Hoecker U, Liu B, Xu L, et al. Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell. 2005; 17: 804–821. doi: 10.1105/tpc.104.030205 15705947

45. Yin R, Arongaus AB, Binkert M, Ulm R. Two distinct domains of the UVR8 photoreceptor interact with COP1 to initiate UV-B signaling in Arabidopsis. Plant Cell. 2015; 27: 202–213. doi: 10.1105/tpc.114.133868 25627067

46. Li L, Zhang Q, Pedmale UV, Nito K, Fu W, Lin L, et al. PIL1 participates in a negative feedback loop that regulates its own gene expression in response to shade. Mol Plant. 2014; 7: 1582–1585. doi: 10.1093/mp/ssu068 24895419

47. Luo Q, Lian HL, He SB, Li L, Jia KP, Yang HQ. COP1 and phyB physically interact with PIL1 to regulate its stability and photomorphogenic development in Arabidopsis. Plant Cell. 2014; 26: 2441–2456. doi: 10.1105/tpc.113.121657 24951480

48. Zhang B, Holmlund M, Lorrain S, Norberg M, Bako L, Fankhauser C, et al. BLADE-ON-PETIOLE proteins act in an E3 ubiquitin ligase complex to regulate PHYTOCHROME INTERACTING FACTOR 4 abundance. Elife. 2017; 6. doi: 10.7554/eLife.26759.001 28826468

49. Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, Lopez-Vidriero I, et al. Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J. 2012; 71: 699–711. doi: 10.1111/j.1365-313X.2012.05033.x 22536829

50. Zhang Y, Mayba O, Pfeiffer A, Shi H, Tepperman JM, Speed TP, et al. 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. 2013; 9: e1003244. doi: 10.1371/journal.pgen.1003244 23382695

51. Xu X, Kathare PK, Pham VN, Bu Q, Nguyen A, Huq E. Reciprocal proteasome-mediated degradation of PIFs and HFR1 underlies photomorphogenic development in Arabidopsis. Development. 2017; 144: 1831–1840. doi: 10.1242/dev.146936 28420710

52. Casal JJ, Balasubramanian S. Thermomorphogenesis. Annu Rev Plant Biol. 2019; 70: 321–346. doi: 10.1146/annurev-arplant-050718-095919 30786235

53. Keller MM, Jaillais Y, Pedmale UV, Moreno JE, Chory J, Ballare CL. Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades. Plant J. 2011; 67: 195–207. doi: 10.1111/j.1365-313X.2011.04598.x 21457375

54. Pedmale UV, Huang SS, Zander M, Cole BJ, Hetzel J, Ljung K, et al. Cryptochromes interact directly with PIFs to control plant growth in limiting blue light. Cell. 2016;164: 233–245. doi: 10.1016/j.cell.2015.12.018 26724867

55. Ma D, Li X, Guo Y, Chu J, Fang S, Yan C, et al. Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light. Proc Natl Acad Sci USA. 2016; 113: 224–229. doi: 10.1073/pnas.1511437113 26699514

56. Huq E, Quail PH. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 2002; 21: 2441–2450. doi: 10.1093/emboj/21.10.2441 12006496

57. Pham VN, Kathare PK, Huq E. Dynamic regulation of PIF5 by COP1-SPA complex to optimize photomorphogenesis in Arabidopsis. Plant J. 2018; 96: 260–273. doi: 10.1111/tpj.14074 30144338

58. Cloix C, Kaiserli E, Heilmann M, Baxter KJ, Brown BA, O'Hara A, et al. C-terminal region of the UV-B photoreceptor UVR8 initiates signaling through interaction with the COP1 protein. Proc Natl Acad Sci USA. 2012; 109: 16366–16370. doi: 10.1073/pnas.1210898109 22988111

59. Salter MG, Franklin KA, Whitelam GC. Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature. 2003; 426: 680–683. doi: 10.1038/nature02174 14668869

60. Galstyan A, Cifuentes-Esquivel N, Bou-Torrent J, Martinez-Garcia JF. The shade avoidance syndrome in Arabidopsis: a fundamental role for atypical basic helix-loop-helix proteins as transcriptional cofactors. Plant J. 2011; 66: 258–267. doi: 10.1111/j.1365-313X.2011.04485.x 21205034

61. Hao Y, Oh E, Choi G, Liang Z, Wang ZY. Interactions between HLH and bHLH factors modulate light-regulated plant development. Mol Plant. 2012; 5: 688–697. doi: 10.1093/mp/sss011 22331621

62. Roig-Villanova I, Bou-Torrent J, Galstyan A, Carretero-Paulet L, Portoles S, Rodriguez-Concepcion M, et al. Interaction of shade avoidance and auxin responses: a role for two novel atypical bHLH proteins. EMBO J. 2007; 26: 4756–4767. doi: 10.1038/sj.emboj.7601890 17948056

63. Moriconi V, Binkert M, Costigliolo C, Sellaro R, Ulm R, Casal JJ. Perception of sunflecks by the UV-B photoreceptor UV RESISTANCE LOCUS8. Plant Physiol. 2018; 177: 75–81. doi: 10.1104/pp.18.00048 29530938

64. Sellaro R, Yanovsky MJ, Casal JJ. Repression of shade-avoidance reactions by sunfleck induction of HY5 expression in Arabidopsis. Plant J. 2011; 68: 919–928. doi: 10.1111/j.1365-313X.2011.04745.x 21848684

65. McNellis TW, von Arnim AG, Araki T, Komeda Y, Misera S, Deng XW. Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell. 1994; 6: 487–500. doi: 10.1105/tpc.6.4.487 8205001

66. Fankhauser C, Chory J. RSF1, an Arabidopsis locus implicated in phytochrome A signaling. Plant Physiol. 2000; 124: 39–45. doi: 10.1104/pp.124.1.39 10982420

67. Sessa G, Carabelli M, Sassi M, Ciolfi A, Possenti M, Mittempergher F, et al. A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev. 2005; 19: 2811–2815. doi: 10.1101/gad.364005 16322556

68. de Wit M, Keuskamp DH, Bongers FJ, Hornitschek P, Gommers CMM, Reinen E, et al. Integration of phytochrome and cryptochrome signals determines plant growth during competition for light. Curr Biol. 2016; 26: 3320–3326. doi: 10.1016/j.cub.2016.10.031 27889265

69. Arongaus AB, Chen S, Pireyre M, Glockner N, Galvao VC, Albert A, et al. Arabidopsis RUP2 represses UVR8-mediated flowering in noninductive photoperiods. Genes Dev. 2018; 32: 1332–1343. doi: 10.1101/gad.318592.118 30254107

70. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25: 402–408. doi: 10.1006/meth.2001.1262 11846609

71. Haring M, Offermann S, Danker T, Horst I, Peterhansel C, Stam M. Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods. 2007; 3: 11. doi: 10.1186/1746-4811-3-11 17892552


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