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The Membrane-Associated Transcription Factor NAC089 Controls ER-Stress-Induced Programmed Cell Death in Plants


Protein folding is fundamentally important for development and responses to environmental stresses in eukaryotes. When excess misfolded proteins are accumulated in the endoplasmic reticulum (ER), the unfolded protein response (UPR) is triggered to promote cell survival through optimizing protein folding, and also promote programmed cell death (PCD) when the stress is severe. However, the link from ER-stress-sensing to PCD is largely unknown. Here, we report the identification of one membrane-associated transcription factor NAC089 as an important regulator of ER stress-induced PCD in plants. We have established a previously unrecognized molecular connection between ER stress sensors and PCD regulators. We have shown that organelle-to-organelle translocation of a transcription factor is important for its function in transcriptional regulation. Our results have provided novel insights into the molecular mechanisms of PCD in plants, especially under ER stress conditions.


Vyšlo v časopise: The Membrane-Associated Transcription Factor NAC089 Controls ER-Stress-Induced Programmed Cell Death in Plants. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004243
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004243

Souhrn

Protein folding is fundamentally important for development and responses to environmental stresses in eukaryotes. When excess misfolded proteins are accumulated in the endoplasmic reticulum (ER), the unfolded protein response (UPR) is triggered to promote cell survival through optimizing protein folding, and also promote programmed cell death (PCD) when the stress is severe. However, the link from ER-stress-sensing to PCD is largely unknown. Here, we report the identification of one membrane-associated transcription factor NAC089 as an important regulator of ER stress-induced PCD in plants. We have established a previously unrecognized molecular connection between ER stress sensors and PCD regulators. We have shown that organelle-to-organelle translocation of a transcription factor is important for its function in transcriptional regulation. Our results have provided novel insights into the molecular mechanisms of PCD in plants, especially under ER stress conditions.


Zdroje

1. LiuJX, HowellSH (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22: 2930–2942.

2. SmithMH, PloeghHL, WeissmanJS (2011) Road to ruin: Targeting proteins for degradation in the endoplasmic reticulum. Science 334: 1086–1090.

3. WalterP, RonD (2011) The unfolded protein response: From stress pathway to homeostatic regulation. Science 334: 1081–1086.

4. RonD, WalterP (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519–529.

5. VitaleA, BostonRS (2008) Endoplasmic reticulum quality control and the unfolded protein response: Insights from plants. Traffic 9: 1581–1588.

6. CoxJS, ShamuCE, WalterP (1993) Transcriptional induction of genes encoding endoplasmic-reticulum resident proteins requires a transmembrane protein-kinase. Cell 73: 1197–1206.

7. ShenXH, EllisRE, LeeK, LiuCY, YangK, et al. (2001) Complementary signaling pathways regulate the unfolded protein response and are required for C-elegans development. Cell 107: 893–903.

8. CalfonM, ZengHQ, UranoF, TillJH, HubbardSR, et al. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92–96.

9. DengY, HumbertS, LiuJX, SrivastavaR, RothsteinSJ, et al. (2011) Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc Natl Acad Sci USA 108: 7247–7252.

10. LuSJ, YangZT, SunL, SunL, SongZT, et al. (2012) Conservation of IRE1-regulated bZIP74 mRNA unconventional splicing in rice (Oryza sativa L.) involved in ER stress responses. Mol Plant 5: 504–514.

11. NagashimaY, MishibaKI, SuzukiE, ShimadaY, IwataY, et al. (2011) Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci Rep 1: 29.

12. MorenoAA, MukhtarMS, BlancoF, BoatwrightJL, MorenoI, et al. (2012) IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PloS One 7: e31944.

13. HayashiS, WakasaY, TakahashiH, KawakatsuT, TakaiwaF (2012) Signal transduction by IRE1-mediated splicing of bZIP50 and other stress sensors in the endoplasmic reticulum stress response of rice. Plant J 69: 946–956.

14. DengY, SrivastavaR, HowellSH (2013) Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis. Proc Natl Acad Sci USA 110: 19633–19638.

15. HardingHP, ZhangYH, RonD (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271–274.

16. HazeK, YoshidaH, YanagiH, YuraT, MoriK (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10: 3787–3799.

17. LiuJX, SrivastavaR, CheP, HowellSH (2007) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51: 897–909.

18. LiuJX, SrivastavaR, CheP, HowellSH (2007) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19: 4111–4119.

19. CheP, BussellJD, ZhouWX, EstavilloGM, PogsonBJ, et al. (2010) Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis. Sci Signal 3 (141) ra69.

20. GaoH, BrandizziF, BenningC, LarkinRM (2008) A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proc Natl Acad Sci USA 105: 16398–16403.

21. TajimaH, IwataY, IwanoM, TakayamaS, KoizumiN (2008) Identification of an Arabidopsis transmembrane bZIP transcription factor involved in the endoplasmic reticulum stress response. Biochem Biophy Res Commun 374: 242–247.

22. SitiaR, BraakmanI (2003) Quality control in the endoplasmic reticulum protein factory. Nature 426: 891–894.

23. TabasI, RonD (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13: 184–190.

24. UranoF, WangXZ, BertolottiA, ZhangYH, ChungP, et al. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664–666.

25. ShoreGC, PapaFR, OakesSA (2011) Signaling cell death from the endoplasmic reticulum stress response. Curr Opin Cell Biol 23: 143–149.

26. HetzC, BernasconiP, FisherJ, LeeAH, BassikMC, et al. (2006) Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1 alpha. Science 312: 572–576.

27. UptonJP, WangL, HanD, WangES, HuskeyNE, et al. (2012) IRE1 alpha cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science 338: 818–822.

28. McCulloughKD, MartindaleJL, KlotzLO, AwTY, HolbrookNJ (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bc12 and perturbing the cellular redox state. Mol Cell Biol 21: 1249–1259.

29. HanJ, BackaSH, HurJ, LinY-H, GildersleeveR, et al. (2013) ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol 15: 481.

30. van DoornWG, BeersEP, DanglJL, Franklin-TongVE, GalloisP, et al. (2011) Morphological classification of plant cell deaths. Cell Death Differ 18: 1241–1246.

31. WatanabeN, LamE (2008) BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis. J Biol Chem 283: 3200–3210.

32. ZuppiniA, NavazioL, MarianiP (2004) Endoplasmic reticulum stress-induced programmed cell death in soybean cells. J Cell Sci 117: 2591–2598.

33. FariaJAQA, ReisPAB, ReisMTB, RosadoGL, PinheiroGL, et al. (2011) The NAC domain-containing protein, GmNAC6, is a downstream component of the ER stress- and osmotic stress-induced NRP-mediated cell-death signaling pathway. BMC Plant Biology 11: 129.

34. AlvesMS, ReisPAB, DadaltoSP, FariaJAQA, FontesEPB, et al. (2011) A novel transcription factor, ERD15 (Early Responsive to Dehydration 15), connects endoplasmic reticulum stress with an osmotic stress-induced cell death signal. J Biol Chem 286: 20020–20030.

35. IshikawaT, WatanabeN, NaganoM, Kawai-YamadaM, LamE (2011) Bax inhibitor-1: a highly conserved endoplasmic reticulum-resident cell death suppressor. Cell Death Differ 18: 1271–1278.

36. Kawai-YamadaM, JinLH, YoshinagaK, HirataA, UchimiyaH (2001) Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax Inhibitor-1 (AtBl-1). Proc Natl Acad Sci USA 98: 12295–12300.

37. Kawai-YamadaM, OhoriY, UchimiyaH (2004) Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell 16: 21–32.

38. SanchezP, ZabalaMD, GrantM (2000) AtBI-1, a plant homologue of Bax Inhibitor-1, suppresses Bax-induced cell death in yeast and is rapidly upregulated during wounding and pathogen challenge. Plant J 21: 393–399.

39. HollienJ, LinJH, LiH, StevensN, WalterP, et al. (2009) Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186: 323–331.

40. MishibaKI, NagashimaY, SuzukiE, HayashiN, OgataY, et al. (2013) Defects in IRE1 enhance cell death and fail to degrade mRNAs encoding secretory pathway proteins in the Arabidopsis unfolded protein response. Proc Natl Acad Sci USA 110: 5713–5718.

41. CostaMDL, ReisPAB, ValenteMAS, IrsiglerAST, CarvalhoCM, et al. (2008) A new branch of endoplasmic reticulum stress signaling and the osmotic signal converge on plant-specific asparagine-rich proteins to promote cell death. J Biol Chem 283: 20209–20219.

42. MendesGC, ReisPAB, CalilIP, CarvalhoHH, AragaoFJL, et al. (2013) GmNAC30 and GmNAC81 integrate the endoplasmic reticulum stress- and osmotic stress-induced cell death responses through a vacuolar processing enzyme. Proc Natl Acad Sci USA 110: 19627–19632.

43. LiuJX, HowellSH (2010) bZIP28 and NF-Y transcription factors are activated by ER Stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell 22: 782–796.

44. IwataY, KoizumiN (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102: 5280–5285.

45. KimSY, KimSG, KimYS, SeoPJ, BaeM, et al. (2007) Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation. Nucl Acid Res 35: 203–213.

46. LiJ, ZhangJ, WangX, ChenJ (2010) A membrane-tethered transcription factor ANAC089 negatively regulates floral initiation in Arabidopsis thaliana. Sci China-Life Sci 53: 1299–1306.

47. HiratsuK, MatsuiK, KoyamaT, Ohme-TakagiM (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34: 733–739.

48. ZuoJR, NiuQW, ChuaNH (2000) An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24: 265–273.

49. PorterAG, JanickeRU (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6: 99–104.

50. HanJJ, LinW, OdaY, CuiKM, FukudaH, et al. (2012) The proteasome is responsible for caspase-3-like activity during xylem development. Plant J 72: 129–141.

51. KuriyamaH, FukudaH (2002) Developmental programmed cell death in plants. Curr Opin Plant Biol 5: 568–573.

52. LamE, KatoN, LawtonM (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411: 848–853.

53. CollNS, VercammenD, SmidlerA, CloverC, Van BreusegemF, et al. (2010) Arabidopsis type I metacaspases control cell death. Science 330: 1393–1397.

54. Ohashi-ItoK, OdaY, FukudaH (2010) Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 22: 3461–3473.

55. LaiZ, WangF, ZhengZ, FanB, ChenZ (2011) A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 66: 953–968.

56. CrostiP, MalerbaM, BianchettiR (2001) Tunicamycin and Brefeldin A induce in plant cells a programmed cell death showing apoptotic features. Protoplasma 216: 31–38.

57. HoeberichtsFA, WolteringEJ (2003) Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators. Bioessays 25: 47–57.

58. EichmannR, SchaferP (2012) The endoplasmic reticulum in plant immunity and cell death. Front Plant Sci 3: 200–200.

59. CacasJL (2010) Devil inside: does plant programmed cell death involve the endomembrane system? Plant Cell Environ 33: 1453–1473.

60. LoveAJ, MilnerJJ, SadanandomA (2008) Timing is everything: regulatory overlap in plant cell death. Trend Plant Sci 13: 589–595.

61. WangS, NarendraS, FedoroffN (2007) Heterotrimeric G protein signaling in the Arabidopsis unfolded protein response. Proc Natl Acad Sci USA 104: 3817–3822.

62. ChenY, BrandizziF (2012) AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis. Plant J 69: 266–277.

63. TsiatsianiL, Van BreusegemF, GalloisP, ZavialovA, LamE, et al. (2011) Metacaspases. Cell Death Differ 18: 1279–1288.

64. LamE, ZhangY (2012) Regulating the reapers: activating metacaspases for programmed cell death. Trend Plant Sci 17: 487–494.

65. YeY, LiZ, XingD (2013) Nitric oxide promotes MPK6-mediated caspase-3-like activation in cadmium-induced Arabidopsis thaliana programmed cell death. Plant Cell Environ 36: 1–15.

66. ZhangL, XuQ, XingD, GaoC, XiongH (2009) Real-time detection of caspase-3-like protease activation in vivo using fluorescence resonance energy transfer during plant programmed cell death Induced by ultraviolet C overexposure. Plant Physiol 150: 1773–1783.

67. DanonA, RotariVI, GordonA, MailhacN, GalloisP (2004) Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and Defender against Apoptotic Death. J Biol Chem 279: 779–787.

68. HatsugaiN, IwasakiS, TamuraK, KondoM, FujiK, et al. (2009) A novel membrane fusion-mediated plant immunity against bacterial pathogens. Gene Dev 23: 2496–2506.

69. TakayamaS, SatoT, KrajewskiS, KochelK, IrieS, et al. (1995) Cloning and functional-anlaysis of BAG-1 - A novel BCL-2-binding protein with anti-cell death activity. Cell 80: 279–284.

70. DoukhaninaEV, ChenS, van der ZalmE, GodzikA, ReedJ, et al. (2006) Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J Biol Chem 281: 18793–18801.

71. KangCH, JungWY, KangYH, KimJY, KimDG, et al. (2006) AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants. Cell Death Differ 13: 84–95.

72. SunL, LuSJ, ZhangSS, ZhouSF, SunL, et al. (2013) The lumen-facing domain is important for the biological function and organelle-to-organelle movement of bZIP28 during ER Stress in Arabidopsis. Mol Plant 6: 1605–1615.

73. SrivastavaR, DengY, ShahS, RaoAG, HowellSH (2013) BINDING PROTEIN is a master regulator of the endoplasmic reticulum stress sensor/transducer bZIP28 in Arabidopsis. Plant Cell 25: 1416–1429.

74. GardnerBM, WalterP (2011) Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science 333: 1891–1894.

75. KimYS, KimSG, ParkJE, ParkHY, LimMH, et al. (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18: 3132–3144.

76. KimSG, LeeAK, YoonHK, ParkCM (2008) A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. Plant J 55: 77–88.

77. NgS, IvanovaA, DuncanO, LawSR, Van AkenO, et al. (2013) A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell 25: 3450–3471.

78. De ClercqI, VermeirssenV, Van AkenO, VandepoeleK, MurchaMW, et al. (2013) The membrane-bound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis. Plant Cell 25: 3472–3490.

79. LiP, WindJJ, ShiX, ZhangH, HansonJ, et al. (2011) Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain. Proc Natl Acad Sci USA 108: 3436–3441.

80. ZhangC, ChenX, ZhuRM, ZhangY, YuT, et al. (2012) Endoplasmic reticulum stress is involved in hepatic SREBP-1c activation and lipid accumulation in fructose-fed mice. Toxi Lett 212: 229–240.

81. KleinP, SeidelT, StockerB, DietzKJ (2012) The membrane-tethered transcription factor ANAC089 serves as redox-dependent suppressor of stromal ascorbate peroxidase gene expression. Front Plant Sci 3: 247–247.

82. LinJH, LiH, YasumuraD, CohenHR, ZhangC, et al. (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318: 944–949.

83. HowellSH (2013) Endoplasmic reticulum stress responses in plants. Annual Rev Plant Biol 64: 477–499.

84. QiangX, ZechmannB, ReitzMU, KogelK-H, SchaeferP (2012) The mutualistic fungus piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. Plant Cell 24: 794–809.

85. LiuY, BurgosJS, DengY, SrivastavaR, HowellSH, et al. (2012) Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis. Plant Cell 24: 4635–4651.

86. SunL, YangZT, SongZT, WangMJ, LuSJ, et al. (2013) The plant-specific transcription factor NAC103 is induced by bZIP60 through a new cis-regulatory element to modulate the unfolded protein response in Arabidopsis. Plant J 76: 274–286.

87. LiuJX, SrivastavaR, HowellSH (2008) Stress-induced expression of an activated form of AtbZIP17 provides protection from salt stress in Arabidopsis. Plant Cell Environ 31: 1735–1743.

88. IwataY, FedoroffNV, KoizumiN (2008) Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20: 3107–3121.

89. HellensRP, AllanAC, FrielEN, BolithoK, GraftonK, et al. (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1: 13.

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