Ethylene Promotes Hypocotyl Growth and HY5 Degradation by Enhancing the Movement of COP1 to the Nucleus in the Light

English version České info

In the dark, etiolated seedlings display a long hypocotyl, the growth of which is rapidly inhibited when the seedlings are exposed to light. In contrast, the phytohormone ethylene prevents hypocotyl elongation in the dark but enhances its growth in the light. However, the mechanism by which light and ethylene signalling oppositely affect this process at the protein level is unclear. Here, we report that ethylene enhances the movement of CONSTITUTIVE PHOTOMORPHOGENESIS 1 (COP1) to the nucleus where it mediates the degradation of LONG HYPOCOTYL 5 (HY5), contributing to hypocotyl growth in the light. Our results indicate that HY5 is required for ethylene-promoted hypocotyl growth in the light, but not in the dark. Using genetic and biochemical analyses, we found that HY5 functions downstream of ETHYLENE INSENSITIVE 3 (EIN3) for ethylene-promoted hypocotyl growth. Furthermore, the upstream regulation of HY5 stability by ethylene is COP1-dependent, and COP1 is genetically located downstream of EIN3, indicating that the COP1-HY5 complex integrates light and ethylene signalling downstream of EIN3. Importantly, the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) enriched the nuclear localisation of COP1; however, this effect was dependent on EIN3 only in the presence of light, strongly suggesting that ethylene promotes the effects of light on the movement of COP1 from the cytoplasm to the nucleus. Thus, our investigation demonstrates that the COP1-HY5 complex is a novel integrator that plays an essential role in ethylene-promoted hypocotyl growth in the light.

Vyšlo v časopise: Ethylene Promotes Hypocotyl Growth and HY5 Degradation by Enhancing the Movement of COP1 to the Nucleus in the Light. PLoS Genet 9(12): e32767. doi:10.1371/journal.pgen.1004025
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004025

Souhrn

Zdroje

1. WangKL, LiH, EckerJR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14 Suppl: S131–151.

2. GuoH, EckerJR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7: 40–49.

3. StepanovaAN, AlonsoJM (2009) Ethylene signaling and response: where different regulatory modules meet. Curr Opin Plant Biol 12: 548–555.

4. HuaJ, MeyerowitzEM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94: 261–271.

5. HuaJ, SakaiH, NourizadehS, ChenQG, BleeckerAB, et al. (1998) EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell 10: 1321–1332.

6. KieberJJ, RothenbergM, RomanG, FeldmannKA, EckerJR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72: 427–441.

7. ClarkKL, LarsenPB, WangX, ChangC (1998) Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc Natl Acad Sci U S A 95: 5401–5406.

8. HuangY, LiH, HutchisonCE, LaskeyJ, KieberJJ (2003) Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J 33: 221–233.

9. JuC, YoonGM, ShemanskyJM, LinDY, YingZI, et al. (2012) CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc Natl Acad Sci U S A 109: 19486–19491.

10. BissonMM, BleckmannA, AllekotteS, GrothG (2009) EIN2, the central regulator of ethylene signalling, is localized at the ER membrane where it interacts with the ethylene receptor ETR1. Biochem J 424: 1–6.

11. JiY, GuoH (2013) From endoplasmic reticulum (ER) to nucleus: EIN2 bridges the gap in ethylene signaling. Mol Plant 6: 11–14.

12. QiaoH, ShenZ, HuangSS, SchmitzRJ, UrichMA, et al. (2012) Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science 338: 390–393.

13. WenX, ZhangC, JiY, ZhaoQ, HeW, et al. (2012) Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus. Cell Res 22: 1613–1616.

14. GuoH, EckerJR (2003) Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115: 667–677.

15. AnF, ZhaoQ, JiY, LiW, JiangZ, et al. (2010) Ethylene-induced stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-box 1 and 2 that requires EIN2 in Arabidopsis. Plant Cell 22: 2384–2401.

16. SolanoR, StepanovaA, ChaoQ, EckerJR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12: 3703–3714.

17. KonishiM, YanagisawaS (2008) Ethylene signaling in Arabidopsis involves feedback regulation via the elaborate control of EBF2 expression by EIN3. Plant J 55: 821–831.

18. ChenH, XueL, ChintamananiS, GermainH, LinH, et al. (2009) ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 21: 2527–2540.

19. ZhongS, ZhaoM, ShiT, ShiH, AnF, et al. (2009) EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings. Proc Natl Acad Sci U S A 106: 21431–21436.

20. BoutrotF, SegonzacC, ChangKN, QiaoH, EckerJR, et al. (2010) Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci U S A 107: 14502–14507.

21. ZhangL, LiZ, QuanR, LiG, WangR, et al. (2011) An AP2 domain-containing gene, ESE1, targeted by the ethylene signaling component EIN3 is important for the salt response in Arabidopsis. Plant Physiol 157: 854–865.

22. von ArnimA, DengXW (1996) Light control of seedling development. Annu Rev Plant Physiol Plant Mol Biol 47: 215–243.

23. CaryAJ, LiuW, HowellSH (1995) Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol 107: 1075–1082.

24. SmalleJ, HaegmanM, KurepaJ, Van MontaguM, StraetenDV (1997) Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proc Natl Acad Sci U S A 94: 2756–2761.

25. LiH, JohnsonP, StepanovaA, AlonsoJM, EckerJR (2004) Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev Cell 7: 193–204.

26. ChenH, ZhangJ, NeffMM, HongSW, ZhangH, et al. (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci U S A 105: 4495–4500.

27. 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.

28. FengS, MartinezC, GusmaroliG, WangY, ZhouJ, et al. (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475–479.

29. LauOS, DengXW (2010) Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol 13: 571–577.

30. BaiMY, ShangJX, OhE, FanM, BaiY, et al. (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14: 810–817.

31. WangQ, ZhuZ, OzkardeshK, LinC (2013) Phytochromes and phytohormones: the shrinking degree of separation. Mol Plant 6: 5–7.

32. CluisCP, MouchelCF, HardtkeCS (2004) The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J 38: 332–347.

33. AngLH, ChattopadhyayS, WeiN, OyamaT, OkadaK, et al. (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1: 213–222.

34. 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.

35. von ArnimAG, DengXW (1994) Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 79: 1035–1045.

36. OsterlundMT, HardtkeCS, WeiN, DengXW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462–466.

37. VandenbusscheF, HabricotY, CondiffAS, MaldineyR, Van der StraetenD, et al. (2007) HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana. Plant J 49: 428–441.

38. AlabadiD, Gallego-BartolomeJ, OrlandoL, Garcia-CarcelL, RubioV, et al. (2008) Gibberellins modulate light signaling pathways to prevent Arabidopsis seedling de-etiolation in darkness. Plant J 53: 324–335.

39. ZhongS, ShiH, XueC, WangL, XiY, et al. (2012) A molecular framework of light-controlled phytohormone action in Arabidopsis. Curr Biol 22: 1530–1535.

40. LiangX, WangH, MaoL, HuY, DongT, et al. (2012) Involvement of COP1 in ethylene- and light-regulated hypocotyl elongation. Planta 236: 1791–1802.

41. 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.

42. JingY, ZhangD, WangX, TangW, WangW, et al. (2013) Arabidopsis chromatin remodeling factor PICKLE interacts with transcription factor HY5 to regulate hypocotyl cell elongation. Plant Cell 25: 242–256.

43. ChaeHS, FaureF, KieberJJ (2003) The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15: 545–559.

44. 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.

45. McNellisTW, von ArnimAG, ArakiT, KomedaY, MiseraS, et al. (1994) Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell 6: 487–500.

46. ToriiKU, McNellisTW, DengXW (1998) Functional dissection of Arabidopsis COP1 reveals specific roles of its three structural modules in light control of seedling development. EMBO J 17: 5577–5587.

47. SeoHS, YangJY, IshikawaM, BolleC, BallesterosML, et al. (2003) LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423: 995–999.

48. YangJ, LinR, SullivanJ, HoeckerU, LiuBX, et al. (2005) Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell 17: 804–821.

49. JangIC, YangJY, SeoHS, ChuaNH (2005) HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev 19: 593–602.

50. SamacDA, HironakaCM, YallalyPE, ShahDM (1990) Isolation and Characterization of the Genes Encoding Basic and Acidic Chitinase in Arabidopsis thaliana. Plant Physiol 93: 907–914.

51. PacinM, LegrisM, CasalJJ (2013) COP1 re-accumulates in the nucleus under shade. Plant J 75: 631–641.

52. SaijoY, SullivanJA, WangH, YangJ, ShenY, et al. (2003) The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev 17: 2642–2647.

53. SubramanianC, KimBH, LyssenkoNN, XuX, JohnsonCH, et al. (2004) The Arabidopsis repressor of light signaling, COP1, is regulated by nuclear exclusion: mutational analysis by bioluminescence resonance energy transfer. Proc Natl Acad Sci U S A 101: 6798–6802.

54. YiC, DengXW (2005) COP1-from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol 15: 618–625.

55. 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.

56. ZhangZ, HuangR (2010) Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis. Plant Mol Biol 73: 241–249.

57. AchardP, ChengH, De GrauweL, DecatJ, SchouttetenH, et al. (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311: 91–94.

58. AlonsoJM, HirayamaT, RomanG, NourizadehS, EckerJR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284: 2148–2152.

59. WangX, LiW, PiquerasR, CaoK, DengXW, et al. (2009) Regulation of COP1 nuclear localization by the COP9 signalosome via direct interaction with CSN1. Plant J 58: 655–667.

60. FranciosiniA, LombardiB, IafrateS, PecceV, MeleG, et al. (2013) The Arabidopsis COP9 SIGNALOSOME INTERACTING F-BOX KELCH 1 protein forms an SCF ubiquitin ligase and regulates hypocotyl elongation. Mol Plant 6: 1616–1629.

61. ChristiansMJ, RoblesLM, ZellerSM, LarsenPB (2008) The eer5 mutation, which affects a novel proteasome-related subunit, indicates a prominent role for the COP9 signalosome in resetting the ethylene-signaling pathway in Arabidopsis. Plant J 55: 467–477.

62. 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.

63. ChapmanEJ, GreenhamK, CastillejoC, SartorR, BialyA, et al. (2012) Hypocotyl transcriptome reveals auxin regulation of growth-promoting genes through GA-dependent and -independent pathways. PLoS One 7: e36210.

64. LiZ, HuangR (2011) The reciprocal regulation of abscisic acid and ethylene biosyntheses. Plant Signal Behav 6: 1647–1650.

65. LiZ, ZhangL, YuY, QuanR, ZhangZ, et al. (2011) The ethylene response factor AtERF11 that is transcriptionally modulated by the bZIP transcription factor HY5 is a crucial repressor for ethylene biosynthesis in Arabidopsis. Plant J 68: 88–99.

66. De GrauweL, ChaerleL, DugardeynJ, DecatJ, RieuI, et al. (2008) Reduced gibberellin response affects ethylene biosynthesis and responsiveness in the Arabidopsis gai eto2-1 double mutant. New Phytol 177: 128–141.

67. JangIC, HenriquesR, SeoHS, NagataniA, ChuaNH (2010) Arabidopsis PHYTOCHROME INTERACTING FACTOR proteins promote phytochrome B polyubiquitination by COP1 E3 ligase in the nucleus. Plant Cell 22: 2370–2383.