Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in

English version České info

Network robustness is a crucial property of the plant immune signaling network because pathogens are under a strong selection pressure to perturb plant network components to dampen plant immune responses. Nevertheless, modulation of network robustness is an area of network biology that has rarely been explored. While two modes of plant immunity, Effector-Triggered Immunity (ETI) and Pattern-Triggered Immunity (PTI), extensively share signaling machinery, the network output is much more robust against perturbations during ETI than PTI, suggesting modulation of network robustness. Here, we report a molecular mechanism underlying the modulation of the network robustness in Arabidopsis thaliana. The salicylic acid (SA) signaling sector regulates a major portion of the plant immune response and is important in immunity against biotrophic and hemibiotrophic pathogens. In Arabidopsis, SA signaling was required for the proper regulation of the vast majority of SA-responsive genes during PTI. However, during ETI, regulation of most SA-responsive genes, including the canonical SA marker gene PR1, could be controlled by SA-independent mechanisms as well as by SA. The activation of the two immune-related MAPKs, MPK3 and MPK6, persisted for several hours during ETI but less than one hour during PTI. Sustained MAPK activation was sufficient to confer SA-independent regulation of most SA-responsive genes. Furthermore, the MPK3 and SA signaling sectors were compensatory to each other for inhibition of bacterial growth as well as for PR1 expression during ETI. These results indicate that the duration of the MAPK activation is a critical determinant for modulation of robustness of the immune signaling network. Our findings with the plant immune signaling network imply that the robustness level of a biological network can be modulated by the activities of network components.

Vyšlo v časopise: Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in. PLoS Genet 9(12): e32767. doi:10.1371/journal.pgen.1004015
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004015

Souhrn

Zdroje

1. MaselJ, SiegalML (2009) Robustness: mechanisms and consequences. Trends Genet 25 : 395–403.

2. ShinarG, FeinbergM (2011) Design principles for robust biochemical reaction networks: what works, what cannot work, and what might almost work. Math Biosci 231 : 39–48.

3. JonesJD, DanglJL (2006) The plant immune system. Nature 444 : 323–329.

4. TsudaK, KatagiriF (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13 : 459–465.

5. SpoelSH, DongX (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12 : 89–100.

6. SchwessingerB, RonaldPC (2012) Plant innate immunity: perception of conserved microbial signatures. Annu Rev Plant Biol 63 : 451–482.

7. 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.

8. HannDR, Gimenez-IbanezS, RathjenJP (2010) Bacterial virulence effectors and their activities. Curr Opin Plant Biol 13 : 388–393.

9. de JongeR, BoltonMD, ThommaBP (2011) How filamentous pathogens co-opt plants: the ins and outs of fungal effectors. Curr Opin Plant Biol 14 : 400–406.

10. TakkenFL, GoverseA (2012) How to build a pathogen detector: structural basis of NB-LRR function. Curr Opin Plant Biol 15 : 375–384.

11. Penaloza-VazquezA, PrestonGM, CollmerA, BenderCL (2000) Regulatory interactions between the Hrp type III protein secretion system and coronatine biosynthesis in Pseudomonas syringae pv. tomato DC3000. Microbiology 146 (Pt 10) 2447–2456.

12. GengX, ChengJ, GangadharanA, MackeyD (2012) The coronatine toxin of Pseudomonas syringae is a multifunctional suppressor of Arabidopsis defense. Plant Cell 24 : 4763–4774.

13. ZhengXY, SpiveyNW, ZengW, LiuPP, FuZQ, et al. (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11 : 587–596.

14. VlotAC, DempseyDA, KlessigDF (2009) Salicylic Acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47 : 177–206.

15. WildermuthMC, DewdneyJ, WuG, AusubelFM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414 : 562–565.

16. DocziR, OkreszL, RomeroAE, PaccanaroA, BogreL (2012) Exploring the evolutionary path of plant MAPK networks. Trends Plant Sci 17 : 518–525.

17. RasmussenMW, RouxM, PetersenM, MundyJ (2012) MAP Kinase Cascades in Arabidopsis Innate Immunity. Front Plant Sci 3 : 169.

18. LiuY, ZhangS (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16 : 3386–3399.

19. LiG, MengX, WangR, MaoG, HanL, et al. (2012) Dual-Level Regulation of ACC Synthase Activity by MPK3/MPK6 Cascade and Its Downstream WRKY Transcription Factor during Ethylene Induction in Arabidopsis. PLoS Genet 8: e1002767.

20. RenD, LiuY, YangKY, HanL, MaoG, et al. (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci U S A 105 : 5638–5643.

21. WangH, NgwenyamaN, LiuY, WalkerJC, ZhangS (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19 : 63–73.

22. DjameiA, PitzschkeA, NakagamiH, RajhI, HirtH (2007) Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science 318 : 453–456.

23. PitzschkeA, DjameiA, TeigeM, HirtH (2009) VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression. Proc Natl Acad Sci U S A 106 : 18414–18419.

24. KatagiriF, TsudaK (2010) Understanding the plant immune system. Mol Plant Microbe Interact 23 : 1531–1536.

25. TsudaK, SatoM, StoddardT, GlazebrookJ, KatagiriF (2009) Network properties of robust immunity in plants. PLoS Genet 5: e1000772.

26. TsudaK, SatoM, GlazebrookJ, CohenJD, KatagiriF (2008) Interplay between MAMP-triggered and SA-mediated defense responses. Plant J 53 : 763–775.

27. UnderwoodW, ZhangS, HeSY (2007) The Pseudomonas syringae type III effector tyrosine phosphatase HopAO1 suppresses innate immunity in Arabidopsis thaliana. Plant J 52 : 658–672.

28. 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.

29. BeckersGJ, JaskiewiczM, LiuY, UnderwoodWR, HeSY, et al. (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21 : 944–953.

30. RenD, YangH, ZhangS (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277 : 559–565.

31. TenaG, BoudsocqM, SheenJ (2011) Protein kinase signaling networks in plant innate immunity. Curr Opin Plant Biol 14 : 519–529.

32. ZipfelC, RobatzekS, NavarroL, OakeleyEJ, JonesJD, et al. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428 : 764–767.

33. RobatzekS, ChinchillaD, BollerT (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20 : 537–542.

34. LuD, LinW, GaoX, WuS, ChengC, et al. (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332 : 1439–1442.

35. BartelsS, Gonzalez BesteiroMA, LangD, UlmR (2010) Emerging functions for plant MAP kinase phosphatases. Trends Plant Sci 15 : 322–329.

36. TraverseS, GomezN, PatersonH, MarshallC, CohenP (1992) Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem J 288 (Pt 2) 351–355.

37. SabbaghWJr, FlatauerLJ, BardwellAJ, BardwellL (2001) Specificity of MAP kinase signaling in yeast differentiation involves transient versus sustained MAPK activation. Mol Cell 8 : 683–691.

38. GlotinAL, CalipelA, BrossasJY, FaussatAM, TretonJ, et al. (2006) Sustained versus transient ERK1/2 signaling underlies the anti -⁠ and proapoptotic effects of oxidative stress in human RPE cells. Invest Ophthalmol Vis Sci 47 : 4614–4623.

39. LeeJ, RuddJJ, MacioszekVK, ScheelD (2004) Dynamic changes in the localization of MAPK cascade components controlling pathogenesis-related (PR) gene expression during innate immunity in parsley. J Biol Chem 279 : 22440–22448.

40. AhlforsR, MacioszekV, RuddJ, BroscheM, SchlichtingR, et al. (2004) Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J 40 : 512–522.

41. ManganS, AlonU (2003) Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci U S A 100 : 11980–11985.

42. Pajerowska-MukhtarKM, WangW, TadaY, OkaN, TuckerCL, et al. (2012) The HSF-like transcription factor TBF1 is a major molecular switch for plant growth-to-defense transition. Curr Biol 22 : 103–112.

43. ZhangY, YangY, FangB, GannonP, DingP, et al. (2010) Arabidopsis snc2-1D activates receptor-like protein-mediated immunity transduced through WRKY70. Plant Cell 22 : 3153–3163.

44. WangD, AmornsiripanitchN, DongX (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2: e123.

45. ZhangJ, ShaoF, LiY, CuiH, ChenL, et al. (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1 : 175–185.

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. WuS, LuD, KabbageM, WeiHL, SwingleB, et al. (2011) Bacterial effector HopF2 suppresses arabidopsis innate immunity at the plasma membrane. Mol Plant Microbe Interact 24 : 585–593.

48. ZhangZ, WuY, GaoM, ZhangJ, KongQ, et al. (2012) Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11 : 253–263.

49. LindebergM, CartinhourS, MyersCR, SchechterLM, SchneiderDJ, et al. (2006) Closing the circle on the discovery of genes encoding Hrp regulon members and type III secretion system effectors in the genomes of three model Pseudomonas syringae strains. Mol Plant Microbe Interact 19 : 1151–1158.

50. WiltonM, SubramaniamR, ElmoreJ, FelsensteinerC, CoakerG, et al. (2010) The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. Proc Natl Acad Sci U S A 107 : 2349–2354.

51. CaoH, GlazebrookJ, ClarkeJD, VolkoS, DongX (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88 : 57–63.

52. MindrinosM, KatagiriF, YuGL, AusubelFM (1994) The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78 : 1089–1099.

53. TsudaK, QiY, Nguyen leV, BethkeG, TsudaY, et al. (2012) An efficient Agrobacterium-mediated transient transformation of Arabidopsis. Plant J 69 : 713–719.

54. IgarashiD, TsudaK, KatagiriF (2012) The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J 71 : 194–204.

55. HeidrichK, WirthmuellerL, TassetC, PouzetC, DeslandesL, et al. (2011) Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334 : 1401–1404.

56. IrizarryRA, HobbsB, CollinF, Beazer-BarclayYD, AntonellisKJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 : 249–264.

57. EisenMB, SpellmanPT, BrownPO, BotsteinD (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95 : 14863–14868.