Salt-Induced Stabilization of EIN3/EIL1 Confers Salinity Tolerance by Deterring ROS Accumulation in

English version České info

High salinity, as a world-wide abiotic stress, restricts root water uptake, damages cell physiology, and limits the productivity of agricultural crops. Ethylene is a major phytohormone that regulates plant development in response to adverse environments, including high salt stress. However, the molecular mechanisms of how ethylene signal exerts its effect and how ethylene signaling is modulated upon salt stress remain to be explored. Here, we report that high salinity induces EIN3/EIL1 protein accumulation and EBF1/2 protein degradation in an EIN2-independent manner. Moreover, the activated EIN3 deters excess ROS accumulation and increases salt tolerance. Transcriptome analysis and functional studies reveal an EIN3-directed gene network in salt stress response. Functional studies of 114 SIED (Salt-Induced and EIN3/EIL1-Dependent) genes identify a novel regulator of ROS dismissal and salt tolerance. This new understanding of ethylene/salt mutual regulation would allow a better manipulation and engineering of EIN3 and its downstream SIED genes to enhance plant tolerance and adaption to salt stress, particularly in those economically important crops in the future.

Vyšlo v časopise: Salt-Induced Stabilization of EIN3/EIL1 Confers Salinity Tolerance by Deterring ROS Accumulation in. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004664
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004664

Souhrn

Zdroje

1. ApseMP, AharonGS, SneddenWA, BlumwaldE (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285 : 1256–1258.

2. BradfordKJ, YangSF (1980) Stress-induced Ethylene Production in the Ethylene-requiring Tomato Mutant Diageotropica. Plant Physiol 65 : 327–330.

3. BleeckerAB, KendeH (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16 : 1–18.

4. EckerJR (1995) The ethylene signal transduction pathway in plants. Science 268 : 667–675.

5. ChenYF, EtheridgeN, SchallerGE (2005) Ethylene signal transduction. Ann Bot 95 : 901–915.

6. ChenYF, RandlettMD, FindellJL, SchallerGE (2002) Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J Biol Chem 277 : 19861–19866.

7. ChangC, KwokSF, BleeckerAB, MeyerowitzEM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262 : 539–544.

8. HuaJ, ChangC, SunQ, MeyerowitzEM (1995) Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269 : 1712–1714.

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

10. 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.

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

12. 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.

13. 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.

14. 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.

15. 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.

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

17. 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.

18. 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.

19. GagneJM, SmalleJ, GingerichDJ, WalkerJM, YooSD, et al. (2004) Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc Natl Acad Sci U S A 101 : 6803–6808.

20. PotuschakT, LechnerE, ParmentierY, YanagisawaS, GravaS, et al. (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two arabidopsis F box proteins: EBF1 and EBF2. Cell 115 : 679–689.

21. van LoonLC, GeraatsBP, LinthorstHJ (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11 : 184–191.

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

23. CaoWH, LiuJ, HeXJ, MuRL, ZhouHL, et al. (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143 : 707–719.

24. LeiG, ShenM, LiZG, ZhangB, DuanKX, et al. (2011) EIN2 regulates salt stress response and interacts with a MA3 domain-containing protein ECIP1 in Arabidopsis. Plant Cell Environ 34 : 1678–1692.

25. JiangC, BelfieldEJ, CaoY, SmithJA, HarberdNP (2013) An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell 25 : 3535–3552.

26. VersluesPE, AgarwalM, Katiyar-AgarwalS, ZhuJ, ZhuJK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45 : 523–539.

27. StepanovaAN, YunJ, LikhachevaAV, AlonsoJM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19 : 2169–2185.

28. HeW, BrumosJ, LiH, JiY, KeM, et al. (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of TAA1/TAR activity in ethylene-directed auxin biosynthesis and root growth in Arabidopsis. Plant Cell 23 : 3944–3960.

29. IsmailA, RiemannM, NickP (2012) The jasmonate pathway mediates salt tolerance in grapevines. J Exp Bot 63 : 2127–2139.

30. ZhangH, HuangZ, XieB, ChenQ, TianX, et al. (2004) The ethylene-, jasmonate-, abscisic acid -⁠ and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220 : 262–270.

31. ZhuZ, AnF, FengY, LiP, XueL, et al. (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci U S A 108 : 12539–12544.

32. ChangKN, ZhongS, WeirauchMT, HonG, PelizzolaM, et al. (2013) Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. Elife 2: e00675.

33. EdenE, NavonR, SteinfeldI, LipsonD, YakhiniZ (2009) GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10 : 48.

34. DavletovaS, SchlauchK, CoutuJ, MittlerR (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139 : 847–856.

35. RizhskyL, DavletovaS, LiangH, MittlerR (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279 : 11736–11743.

36. VogelJT, ZarkaDG, Van BuskirkHA, FowlerSG, ThomashowMF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41 : 195–211.

37. SakamotoH, MaruyamaK, SakumaY, MeshiT, IwabuchiM, et al. (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136 : 2734–2746.

38. SunJ, JiangH, XuY, LiH, WuX, et al. (2007) The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48 : 1148–1158.

39. SatoT, MaekawaS, YasudaS, SonodaY, KatohE, et al. (2009) CNI1/ATL31, a RING-type ubiquitin ligase that functions in the carbon/nitrogen response for growth phase transition in Arabidopsis seedlings. Plant J 60 : 852–864.

40. KrepsJA, WuY, ChangHS, ZhuT, WangX, et al. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130 : 2129–2141.

41. HiragaS, YamamotoK, ItoH, SasakiK, MatsuiH, et al. (2000) Diverse expression profiles of 21 rice peroxidase genes. FEBS Lett 471 : 245–250.

42. SchopferP, PlachyC, FrahryG (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol 125 : 1591–1602.

43. 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.

44. ZhouF, AndersenCH, BurhenneK, FischerPH, CollingeDB, et al. (2000) Proton extrusion is an essential signalling component in the HR of epidermal single cells in the barley-powdery mildew interaction. Plant J 23 : 245–254.

45. GadjevI, VanderauweraS, GechevTS, LaloiC, MinkovIN, et al. (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141 : 436–445.

46. ShiY, TianS, HouL, HuangX, ZhangX, et al. (2012) Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 24 : 2578–2595.

47. 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.

48. LingamS, MohrbacherJ, BrumbarovaT, PotuschakT, Fink-StraubeC, et al. (2011) Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell 23 : 1815–1829.

49. ZhaoQ, GuoHW (2011) Paradigms and paradox in the ethylene signaling pathway and interaction network. Mol Plant 4 : 626–634.

50. LiuZ, WuY, YangF, ZhangY, ChenS, et al. (2013) BIK1 interacts with PEPRs to mediate ethylene-induced immunity. Proc Natl Acad Sci U S A 110 : 6205–6210.

51. YanagisawaS, YooSD, SheenJ (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425 : 521–525.

52. 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.

53. WuL, ZhangZ, ZhangH, WangXC, HuangR (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiol 148 : 1953–1963.

54. ApelK, HirtH (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55 : 373–399.

55. RoxasVP, LodhiSA, GarrettDK, MahanJR, AllenRD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41 : 1229–1234.

56. TsengMJ, LiuCW, YiuJC (2007) Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. Plant Physiol Biochem 45 : 822–833.

57. BadawiGH, KawanoN, YamauchiY, ShimadaE, SasakiR, et al. (2004) Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiol Plant 121 : 231–238.

58. De BoerK, TillemanS, PauwelsL, Vanden BosscheR, De SutterV, et al. (2011) APETALA2/ETHYLENE RESPONSE FACTOR and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis. Plant J 66 : 1053–1065.

59. ShyuC, FigueroaP, DepewCL, CookeTF, SheardLB, et al. (2012) JAZ8 lacks a canonical degron and has an EAR motif that mediates transcriptional repression of jasmonate responses in Arabidopsis. Plant Cell 24 : 536–550.

60. LiZ, PengJ, WenX, GuoH (2013) Ethylene-insensitive3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 25 : 3311–3328.

61. JeffersonRA, KavanaghTA, BevanMW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6 : 3901–3907.

62. PengJY, LiZH, XiangH, HuangJH, JiaSH, et al. (2005) Preliminary studies on differential defense responses induced during plant communication. Cell Res 15 : 187–192.

63. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 : 735–743.