Protein Poly(ADP-ribosyl)ation Regulates Immune Gene Expression and Defense Responses

English version České info

Fine-tuning of gene expression is a key feature of successful immune responses. However, the underlying mechanisms are not fully understood. Through a genetic screen in model plant Arabidopsis, we reveal that protein poly(ADP-ribosyl)ation (PARylation) post-translational modification plays a pivotal role in controlling plant immune gene expression and defense to pathogen attacks. PARylation is primarily mediated by poly(ADP-ribose) polymerase (PARP), which transfers ADP-ribose moieties from NAD+ to acceptor proteins. The covalently attached poly(ADP-ribose) polymers on the accept proteins could be hydrolyzed by poly(ADP-ribose) glycohydrolase (PARG). We further show that members of Arabidopsis PARPs and PARGs possess differential in vivo and in vitro enzymatic activities. Importantly, the Arabidopsis parp mutant displayed reduced, whereas parg mutant displayed enhanced, immune gene activation and immunity to pathogen infection. Moreover, Arabidopsis PARP2 activity is elevated upon pathogen signal perception. Compared to the lethality of their mammalian counterparts, the viability and normal growth of Arabidopsis parp and parg null mutants provide a unique genetic system to understand protein PARylation in diverse biological processes at the whole organism level.

Vyšlo v časopise: Protein Poly(ADP-ribosyl)ation Regulates Immune Gene Expression and Defense Responses. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004936
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004936

Souhrn

Zdroje

1. BollerT, FelixG (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60 : 379–406.

2. DoddsPN, RathjenJP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11 : 539–548.

3. MachoAP, ZipfelC (2014) Plant PRRs and the activation of innate immune signaling. Mol Cell 54 : 263–272.

4. ChinchillaD, BauerZ, RegenassM, BollerT, FelixG (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18 : 465–476.

5. Gomez-GomezL, BollerT (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5 : 1003–1011.

6. HeeseA, HannDR, Gimenez-IbanezS, JonesAM, HeK, et al. (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci U S A 104 : 12217–12222.

7. ChinchillaD, ZipfelC, RobatzekS, KemmerlingB, NurnbergerT, et al. (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448 : 497–500.

8. SchulzeB, MentzelT, JehleAK, MuellerK, BeelerS, et al. (2010) Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem 285 : 9444–9451.

9. SunY, LiL, MachoAP, HanZ, HuZ, et al. (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342 : 624–628.

10. LuD, WuS, GaoX, ZhangY, ShanL, et al. (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci U S A 107 : 496–501.

11. ZhangJ, LiW, XiangT, LiuZ, LalukK, et al. (2010) Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7 : 290–301.

12. LinW, LiB, LuD, ChenS, ZhuN, et al. (2014) Tyrosine phosphorylation of protein kinase complex BAK1/BIK1 mediates Arabidopsis innate immunity. Proc Natl Acad Sci U S A 111 : 3632–3637.

13. XuJH, WeiXC, YanLM, LiuD, MaYY, et al. (2013) Identification and functional analysis of phosphorylation residues of the Arabidopsis BOTRYTIS-INDUCED KINASE1. Protein & Cell 4 : 771–781.

14. RouxM, SchwessingerB, AlbrechtC, ChinchillaD, JonesA, et al. (2011) The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23 : 2440–2455.

15. PostelS, KufnerI, BeuterC, MazzottaS, SchwedtA, et al. (2010) The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur J Cell Biol 89 : 169–174.

16. 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.

17. LiJ, WenJ, LeaseKA, DokeJT, TaxFE, et al. (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110 : 213–222.

18. NamKH, LiJ (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110 : 203–212.

19. LinW, LuD, GaoX, JiangS, MaX, et al. (2013) Inverse modulation of plant immune and brassinosteroid signaling pathways by the receptor-like cytoplasmic kinase BIK1. Proc Natl Acad Sci U S A 110 : 12114–12119.

20. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, et al.. (2014) Direct Regulation of the NADPH Oxidase RBOHD by the PRR-Associated Kinase BIK1 during Plant Immunity. Mol Cell.

21. LiL, LiM, YuL, ZhouZ, LiangX, et al. (2014) The FLS2-Associated Kinase BIK1 Directly Phosphorylates the NADPH Oxidase RbohD to Control Plant Immunity. Cell Host Microbe 15 : 329–338.

22. LuoX, KrausWL (2012) On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev 26 : 417–432.

23. BriggsAG, BentAF (2011) Poly(ADP-ribosyl)ation in plants. Trends Plant Sci 16 : 372–380.

24. KalischT, AmeJC, DantzerF, SchreiberV (2012) New readers and interpretations of poly(ADP-ribosyl)ation. Trends Biochem Sci 37 : 381–390.

25. KrausWL, LisJT (2003) PARP goes transcription. Cell 113 : 677–683.

26. GibsonBA, KrausWL (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nature Reviews Molecular Cell Biology 13 : 411–424.

27. KimIK, KieferJR, HoCM, StegemanRA, ClassenS, et al. (2012) Structure of mammalian poly(ADP-ribose) glycohydrolase reveals a flexible tyrosine clasp as a substrate-binding element. Nat Struct Mol Biol 19 : 653–656.

28. SladeD, DunstanMS, BarkauskaiteE, WestonR, LafiteP, et al. (2011) The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature 477 : 616–620.

29. LambRS, CitarelliM, TeotiaS (2012) Functions of the poly(ADP-ribose) polymerase superfamily in plants. Cell Mol Life Sci 69 : 175–189.

30. BoltzKA, JastiM, TownleyJM, ShippenDE (2014) Analysis of poly(ADP-Ribose) polymerases in Arabidopsis telomere biology. PLoS One 9: e88872.

31. JiaQ, den Dulk-RasA, ShenH, HooykaasPJ, de PaterS (2013) Poly(ADP-ribose)polymerases are involved in microhomology mediated back-up non-homologous end joining in Arabidopsis thaliana. Plant Mol Biol 82 : 339–351.

32. SchulzP, JansseuneK, DegenkolbeT, MeretM, ClaeysH, et al. (2014) Poly(ADP-ribose)polymerase activity controls plant growth by promoting leaf cell number. PLoS One 9: e90322.

33. De BlockM, VerduynC, De BrouwerD, CornelissenM (2005) Poly(ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. Plant J 41 : 95–106.

34. VanderauweraS, De BlockM, Van de SteeneN, van de CotteB, MetzlaffM, et al. (2007) Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci U S A 104 : 15150–15155.

35. PandaS, PoirierGG, KaySA (2002) tej defines a role for poly(ADP-ribosyl)ation in establishing period length of the arabidopsis circadian oscillator. Dev Cell 3 : 51–61.

36. Adams-PhillipsL, WanJ, TanX, DunningFM, MeyersBC, et al. (2008) Discovery of ADP-ribosylation and other plant defense pathway elements through expression profiling of four different Arabidopsis-Pseudomonas R-avr interactions. Mol Plant Microbe Interact 21 : 646–657.

37. Adams-PhillipsL, BriggsAG, BentAF (2010) Disruption of Poly(ADP-ribosyl)ation Mechanisms Alters Responses of Arabidopsis to Biotic Stress. Plant Physiology 152 : 267–280.

38. LiGJ, NasarV, YangYX, LiW, LiuB, et al. (2011) Arabidopsis poly(ADP-ribose) glycohydrolase 1 is required for drought, osmotic and oxidative stress responses. Plant Science 180 : 283–291.

39. AsaiT, TenaG, PlotnikovaJ, WillmannMR, ChiuWL, et al. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415 : 977–983.

40. HeP, ShanL, LinNC, MartinGB, KemmerlingB, et al. (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125 : 563–575.

41. LunaE, PastorV, RobertJ, FlorsV, Mauch-ManiB, et al. (2011) Callose deposition: a multifaceted plant defense response. Mol Plant Microbe Interact 24 : 183–193.

42. AravindL, KooninEV (2000) SAP -⁠ a putative DNA-binding motif involved in chromosomal organization. Trends Biochem Sci 25 : 112–114.

43. Le MayN, IltisI, AmeJC, ZhovmerA, BiardD, et al. (2012) Poly (ADP-ribose) glycohydrolase regulates retinoic acid receptor-mediated gene expression. Mol Cell 48 : 785–798.

44. KrishnakumarR, GambleMJ, FrizzellKM, BerrocalJG, KininisM, et al. (2008) Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science 319 : 819–821.

45. KrishnakumarR, KrausWL (2010) PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol Cell 39 : 736–749.

46. WangY, LiJ, HouS, WangX, LiY, et al. (2010) A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22 : 2033–2044.

47. FuZQ, GuoM, JeongBR, TianF, ElthonTE, et al. (2007) A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447 : 284–288.

48. de MurciaJMN, RicoulM, TartierL, NiedergangC, HuberA, et al. (2003) Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. Embo Journal 22 : 2255–2263.

49. KohDW, LawlerAM, PoitrasMF, SasakiM, WattlerS, et al. (2004) Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc Natl Acad Sci U S A 101 : 17699–17704.

50. HanaiS, KanaiM, OhashiS, OkamotoK, YamadaM, et al. (2004) Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc Natl Acad Sci U S A 101 : 82–86.

51. SongJ, BentAF (2014) Microbial pathogens trigger host DNA double-strand breaks whose abundance is reduced by plant defense responses. PLoS Pathog 10: e1004030.

52. TollerIM, NeelsenKJ, StegerM, HartungML, HottigerMO, et al. (2011) Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc Natl Acad Sci U S A 108 : 14944–14949.

53. YanS, WangW, MarquesJ, MohanR, SalehA, et al. (2013) Salicylic acid activates DNA damage responses to potentiate plant immunity. Mol Cell 52 : 602–610.

54. Cohen-ArmonM, VisochekL, RozensalD, KalalA, GeistrikhI, et al. (2007) DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol Cell 25 : 297–308.

55. KrausWL, HottigerMO (2013) PARP-1 and gene regulation: progress and puzzles. Mol Aspects Med 34 : 1109–1123.

56. HeP, ShanL, SheenJ (2007) The use of protoplasts to study innate immune responses. Methods Mol Biol 354 : 1–9.

57. KinkemaM, FanW, DongX (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12 : 2339–2350.