EDR1 Physically Interacts with MKK4/MKK5 and Negatively Regulates a MAP Kinase Cascade to Modulate Plant Innate Immunity

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Plant immunity must be tightly regulated, as over -⁠ or constitutive activation of plant defenses can cause detrimental effects, such as dwarf stature and enhanced cell death. EDR1, a Raf-like mitogen-activated protein kinase (MAPK) kinase kinase, negatively regulates defenses in Arabidopsis. The highly conserved MAPK cascades modulate diverse biological processes, including plant immunity. However, whether EDR1 affects the regulation of one of the MAPK pathways was not previously known. Here, we show that EDR1 physically associates with MKK4 and MKK5, two MAP kinase kinases, and negatively regulates the protein levels of MKK4, MKK5, MPK3 and MPK6. We further show that edr1-mediated disease resistance requires MKK4, MKK5 and MPK3 function. Over-expression of MKK4 or MKK5 in wild-type increased resistance to powdery mildew and caused mildew-induced cell death. Our study suggests that EDR1 negatively regulates defenses and directly modulates the MKK4/MKK5-MPK3/MPK6 cascade to fine-tune plant immunity.

Vyšlo v časopise: EDR1 Physically Interacts with MKK4/MKK5 and Negatively Regulates a MAP Kinase Cascade to Modulate Plant Innate Immunity. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004389
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004389

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Zdroje

1. MengX, ZhangS (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51 : 245–266.

2. InnesRW (2001) Mapping out the roles of MAP Kinases in plant defense. Trends Plant Sci 6 : 392–395.

3. RodriguezMC, PetersenM, MundyJ (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61 : 621–649.

4. AlbrechtC, BoutrotF, SegonzacC, SchwessingerB, Gimenez-IbanezS, et al. (2012) Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc Natl Acad Sci U S A 109 : 303–308.

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

6. 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.

7. DesikanR, HancockJT, IchimuraK, ShinozakiK, NeillSJ (2001) Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6. Plant Physiol 126 : 1579–1587.

8. NuhseTS, PeckSC, HirtH, BollerT (2000) Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK 6. J Biol Chem 275 : 7521–7526.

9. MiyaA, AlbertP, ShinyaT, DesakiY, IchimuraK, et al. (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci U S A 104 : 19613–19618.

10. ZhengZ, QamarSA, ChenZ, MengisteT (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48 : 592–605.

11. 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.

12. MaoG, MengX, LiuY, ZhengZ, ChenZ, et al. (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23 : 1639–1653.

13. 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.

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

15. 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.

16. 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.

17. XiangT, ZongN, ZouY, WuY, ZhangJ, et al. (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18 : 74–80.

18. ShanL, HeP, LiJ, HeeseA, PeckSC, et al. (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4 : 17–27.

19. 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.

20. GoehreV, SpallekT, HaewekerH, MersmannS, MentzelT, et al. (2008) Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Current Biology 18 : 1824–1832.

21. SchweighoferA, KazanaviciuteV, ScheiklE, TeigeM, DocziR, et al. (2007) The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell 19 : 2213–2224.

22. BrockAK, WillmannR, KolbD, GrefenL, LajunenHM, et al. (2010) The Arabidopsis mitogen-activated protein kinase phosphatase PP2C5 affects seed germination, stomatal aperture, and abscisic acid-inducible gene expression. Plant Physiol 153 : 1098–1111.

23. BartelsS, AndersonJC, Gonzalez BesteiroMA, CarreriA, HirtH, et al. (2009) MAP kinase phosphatase1 and protein tyrosine phosphatase1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell 21 : 2884–2897.

24. LeeJS, EllisBE (2007) Arabidopsis MAPK phosphatase 2 (MKP2) positively regulates oxidative stress tolerance and inactivates the MPK3 and MPK6 MAPKs. J Biol Chem 282 : 25020–25029.

25. LumbrerasV, VilelaB, IrarS, SoleM, CapelladesM, et al. (2010) MAPK phosphatase MKP2 mediates disease responses in Arabidopsis and functionally interacts with MPK3 and MPK6. Plant J 63 : 1017–1030.

26. FryeCA, InnesRW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10 : 947–956.

27. PanH, LiuS, TangD (2011) HPR1, a component of the THO/TREX complex, plays an important role in disease resistance and senescence in Arabidopsis. Plant J 69 : 831–843.

28. FryeCA, TangD, InnesRW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci U S A 98 : 373–378.

29. TangD, InnesRW (2002) Overexpression of a kinase-deficient form of the EDR1 gene enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J 32 : 975–983.

30. WawrzynskaA, ChristiansenKM, LanY, RodibaughNL, InnesRW (2008) Powdery mildew resistance conferred by loss of the ENHANCED DISEASE RESISTANCE1 protein kinase is suppressed by a missense mutation in KEEP ON GOING, a regulator of abscisic acid signaling. Plant Physiol 148 : 1510–1522.

31. GuY, InnesRW (2011) The KEEP ON GOING protein of Arabidopsis recruits the ENHANCED DISEASE RESISTANCE1 protein to trans-golgi network/early endosome vesicles. Plant Physiology 155 : 1827–1838.

32. 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.

33. YooSD, ChoYH, TenaG, XiongY, SheenJ (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451 : 789–795.

34. van HultenM, PelserM, van LoonLC, PieterseCM, TonJ (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci U S A 103 : 5602–5607.

35. ObayashiT, HayashiS, SaekiM, OhtaH, KinoshitaK (2009) ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res 37: D987–991.

36. ManfieldIW, JenCH, PinneyJW, MichalopoulosI, BradfordJR, et al. (2006) Arabidopsis Co-expression Tool (ACT): web server tools for microarray-based gene expression analysis. Nucleic Acids Res 34: W504–509.

37. BoudsocqM, WillmannMR, McCormackM, LeeH, ShanL, et al. (2010) Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464 : 418–422.

38. MengX, WangH, HeY, LiuY, WalkerJC, et al. (2012) A MAPK cascade downstream of ERECTA receptor-like protein kinase regulates Arabidopsis inflorescence architecture by promoting localized cell proliferation. Plant Cell 24 : 4948–4960.

39. LukowitzW, RoederA, ParmenterD, SomervilleC (2004) A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116 : 109–119.

40. LuC, HanMH, Guevara-GarciaA, FedoroffNV (2002) Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid. Proc Natl Acad Sci U S A 99 : 15812–15817.

41. YaoC, WuY, NieH, TangD (2012) RPN1a, a 26S proteasome subunit, is required for innate immunity in Arabidopsis. Plant J 71 : 1015–1028.

42. 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.

43. IchimuraK, ShinozakiK, TenaG, SheenJ, HenryY, et al. (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7 : 301–308.

44. 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.

45. 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.

46. BonardiV, TangS, StallmannA, RobertsM, CherkisK, et al. (2011) Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc Natl Acad Sci U S A 108 : 16463–16468.

47. PalmaK, ThorgrimsenS, MalinovskyFG, FiilBK, NielsenHB, et al. (2010) Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor. PLoS Pathog 6: e1001137.

48. TillBJ, ReynoldsSH, GreeneEA, CodomoCA, EnnsLC, et al. (2003) Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res 13 : 524–530.

49. ShiH, ShenQ, QiY, YanH, NieH, et al. (2013) BR-SIGNALING KINASE1 physically associates with FLAGELLIN SENSING2 and regulates plant innate immunity in Arabidopsis. Plant Cell 25 : 1143–1157.

50. WangY, NishimuraMT, ZhaoT, TangD (2011) ATG2, an autophagy-related protein, negatively affects powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant J 68 : 74–87.

51. NieH, ZhaoC, WuG, WuY, ChenY, et al. (2012) SR1, a calmodulin-binding transcription factor, modulates plant defense and ethylene-induced senescence by directly regulating NDR1 and EIN3. Plant Physiol 158 : 1847–1859.

52. LiX, ClarkeJD, ZhangY, DongX (2001) Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol Plant Microbe Interact 14 : 1131–1139.

53. Bracha-DroriK, ShichrurK, KatzA, OlivaM, AngeloviciR, et al. (2004) Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J 40 : 419–427.