Arabidopsis LIP5, a Positive Regulator of Multivesicular Body Biogenesis, Is a Critical Target of Pathogen-Responsive MAPK Cascade in Plant Basal Defense
Pathogen- and stress-responsive mitogen-activated protein kinases 3 and 6 (MPK3/6) cascade plays an important role in plant basal resistance to microbial pathogens. Here we showed that Arabidopsis MPK3 and MPK6 interact with and phosphorylate the LIP5 positive regulator of biogenesis of multivesicular bodies (MVBs), which are unique organelles containing small vesicles in their lumen. Disruption of LIP5 causes increased susceptibility to the bacterial pathogen Pseudomonas syringae. Compromised disease resistance of the lip5 mutants is associated with competent flg22- and salicylic acid-induced defense responses but compromised accumulation of intracellular MVBs and exosome-like paramural vesicles, which have previously been shown to be involved in the relocalization of defense-related molecules. Phosphorylation by MPK3/6 increases LIP5 stability, which is necessary for pathogen-induced MVB trafficking and basal disease resistance. Based on these results we conclude that the MVB pathway is positively regulated by pathogen-responsive MPK3/6 through LIP5 phosphorylation and plays a critical role in plant immune system probably through involvement in the relocalization of defense-related molecules.
Vyšlo v časopise:
Arabidopsis LIP5, a Positive Regulator of Multivesicular Body Biogenesis, Is a Critical Target of Pathogen-Responsive MAPK Cascade in Plant Basal Defense. PLoS Pathog 10(7): e32767. doi:10.1371/journal.ppat.1004243
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004243
Souhrn
Pathogen- and stress-responsive mitogen-activated protein kinases 3 and 6 (MPK3/6) cascade plays an important role in plant basal resistance to microbial pathogens. Here we showed that Arabidopsis MPK3 and MPK6 interact with and phosphorylate the LIP5 positive regulator of biogenesis of multivesicular bodies (MVBs), which are unique organelles containing small vesicles in their lumen. Disruption of LIP5 causes increased susceptibility to the bacterial pathogen Pseudomonas syringae. Compromised disease resistance of the lip5 mutants is associated with competent flg22- and salicylic acid-induced defense responses but compromised accumulation of intracellular MVBs and exosome-like paramural vesicles, which have previously been shown to be involved in the relocalization of defense-related molecules. Phosphorylation by MPK3/6 increases LIP5 stability, which is necessary for pathogen-induced MVB trafficking and basal disease resistance. Based on these results we conclude that the MVB pathway is positively regulated by pathogen-responsive MPK3/6 through LIP5 phosphorylation and plays a critical role in plant immune system probably through involvement in the relocalization of defense-related molecules.
Zdroje
1. ReyesFC, BuonoR, OteguiMS (2011) Plant endosomal trafficking pathways. Current opinion in plant biology 14: 666–673.
2. ContentoAL, BasshamDC (2012) Structure and function of endosomes in plant cells. Journal of cell science 125: 3511–3518.
3. WinterV, HauserMT (2006) Exploring the ESCRTing machinery in eukaryotes. Trends in plant science 11: 115–123.
4. BabstM, WendlandB, EstepaEJ, EmrSD (1998) The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. The EMBO journal 17: 2982–2993.
5. AzmiI, DaviesB, DimaanoC, PayneJ, EckertD, et al. (2006) Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1. The Journal of cell biology 172: 705–717.
6. FujitaH, UmezukiY, ImamuraK, IshikawaD, UchimuraS, et al. (2004) Mammalian class E Vps proteins, SBP1 and mVps2/CHMP2A, interact with and regulate the function of an AAA-ATPase SKD1/Vps4B. Journal of cell science 117: 2997–3009.
7. LottridgeJM, FlanneryAR, VincelliJL, StevensTH (2006) Vta1p and Vps46p regulate the membrane association and ATPase activity of Vps4p at the yeast multivesicular body. Proceedings of the National Academy of Sciences of the United States of America 103: 6202–6207.
8. ScottA, ChungHY, Gonciarz-SwiatekM, HillGC, WhitbyFG, et al. (2005) Structural and mechanistic studies of VPS4 proteins. The EMBO journal 24: 3658–3669.
9. ShiflettSL, WardDM, HuynhD, VaughnMB, SimmonsJC, et al. (2004) Characterization of Vta1p, a class E Vps protein in Saccharomyces cerevisiae. The Journal of biological chemistry 279: 10982–10990.
10. WardDM, VaughnMB, ShiflettSL, WhitePL, PollockAL, et al. (2005) The role of LIP5 and CHMP5 in multivesicular body formation and HIV-1 budding in mammalian cells. The Journal of biological chemistry 280: 10548–10555.
11. YeoSC, XuL, RenJ, BoultonVJ, WagleMD, et al. (2003) Vps20p and Vta1p interact with Vps4p and function in multivesicular body sorting and endosomal transport in Saccharomyces cerevisiae. Journal of cell science 116: 3957–3970.
12. HaasTJ, SliwinskiMK, MartinezDE, PreussM, EbineK, et al. (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. The Plant cell 19: 1295–1312.
13. JonesJD, DanglJL (2006) The plant immune system. Nature 444: 323–329.
14. ChoiSW, TamakiT, EbineK, UemuraT, UedaT, et al. (2013) RABA members act in distinct steps of subcellular trafficking of the FLAGELLIN SENSING2 receptor. The Plant cell 25: 1174–1187.
15. RobatzekS, ChinchillaD, BollerT (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes & development 20: 537–542.
16. BeckM, ZhouJ, FaulknerC, MacLeanD, RobatzekS (2012) Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. The Plant cell 24: 4205–4219.
17. SpallekT, BeckM, Ben KhaledS, SalomonS, BourdaisG, et al. (2013) ESCRT-I mediates FLS2 endosomal sorting and plant immunity. PLoS genetics 9: e1004035.
18. EngelhardtS, BoevinkPC, ArmstrongMR, RamosMB, HeinI, et al. (2012) Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response. The Plant cell 24: 5142–5158.
19. AnQ, EhlersK, KogelKH, van BelAJ, HuckelhovenR (2006) Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. The New phytologist 172: 563–576.
20. AnQ, HuckelhovenR, KogelKH, van BelAJ (2006) Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cellular microbiology 8: 1009–1019.
21. BohleniusH, MorchSM, GodfreyD, NielsenME, Thordal-ChristensenH (2010) The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ROR2 syntaxin-dependent preinvasive basal defense in barley. The Plant cell 22: 3831–3844.
22. MeyerD, PajonkS, MicaliC, O'ConnellR, Schulze-LefertP (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. The Plant journal : for cell and molecular biology 57: 986–999.
23. NielsenME, FeechanA, BohleniusH, UedaT, Thordal-ChristensenH (2012) Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proceedings of the National Academy of Sciences of the United States of America 109: 11443–11448.
24. UnderwoodW, SomervilleSC (2013) Perception of conserved pathogen elicitors at the plasma membrane leads to relocalization of the Arabidopsis PEN3 transporter. Proceedings of the National Academy of Sciences of the United States of America 110: 12492–12497.
25. SpitzerC, ReyesFC, BuonoR, SliwinskiMK, HaasTJ, et al. (2009) The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. The Plant cell 21: 749–766.
26. RobinsonDG, ScheuringD, NaramotoS, FrimlJ (2011) ARF1 localizes to the golgi and the trans-golgi network. The Plant cell 23: 846–849; author reply 849–850.
27. PitzschkeA, SchikoraA, HirtH (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12: 421–426.
28. ZhangS, KlessigDF (2000) Pathogen-induced MAP kinases in tobacco. Results and problems in cell differentiation 27: 65–84.
29. 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 genetics 8: e1002767.
30. MaoG, MengX, LiuY, ZhengZ, ChenZ, et al. (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. The Plant cell 23: 1639–1653.
31. BethkeG, UnthanT, UhrigJF, PoschlY, GustAA, et al. (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proceedings of the National Academy of Sciences of the United States of America 106: 8067–8072.
32. MengX, XuJ, HeY, YangKY, MordorskiB, et al. (2013) Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. The Plant cell 25: 1126–1142.
33. SorenssonC, LenmanM, Veide-VilgJ, SchopperS, LjungdahlT, et al. (2012) Determination of primary sequence specificity of Arabidopsis MAPKs MPK3 and MPK6 leads to identification of new substrates. The Biochemical journal 446: 271–278.
34. LampardGR, MacalisterCA, BergmannDC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322: 1113–1116.
35. FeilnerT, HultschigC, LeeJ, MeyerS, ImminkRG, et al. (2005) High throughput identification of potential Arabidopsis mitogen-activated protein kinases substrates. Molecular & cellular proteomics : MCP 4: 1558–1568.
36. PopescuSC, PopescuGV, BachanS, ZhangZ, GersteinM, et al. (2009) MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes & development 23: 80–92.
37. ConsortiumAIM (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333: 601–607.
38. 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.
39. WildermuthMC, DewdneyJ, WuG, AusubelFM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562–565.
40. ZhengZ, QualleyA, FanB, DudarevaN, ChenZ (2009) An Important Role of a BAHD Acyl Transferase-like Protein in Plant Innate Immunity. Plant J 57: 1040–1053.
41. XiaoJ, XiaH, ZhouJ, AzmiIF, DaviesBA, et al. (2008) Structural basis of Vta1 function in the multivesicular body sorting pathway. Developmental cell 14: 37–49.
42. KimCY, ZhangS (2004) Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco. Plant J 38: 142–151.
43. YangKY, LiuY, ZhangS (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proceedings of the National Academy of Sciences of the United States of America 98: 741–746.
44. ZhangS, LiuY (2001) Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco. The Plant cell 13: 1877–1889.
45. KinoshitaE, Kinoshita-KikutaE, TakiyamaK, KoikeT (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Molecular & cellular proteomics : MCP 5: 749–757.
46. BollerT, FelixG (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual review of plant biology 60: 379–406.
47. VlotAC, DempseyDA, KlessigDF (2009) Salicylic Acid, a multifaceted hormone to combat disease. Annual review of phytopathology 47: 177–206.
48. ZipfelC (2009) Early molecular events in PAMP-triggered immunity. Current opinion in plant biology 12: 414–420.
49. PfundC, Tans-KerstenJ, DunningFM, AlonsoJM, EckerJR, et al. (2004) Flagellin is not a major defense elicitor in Ralstonia solanacearum cells or extracts applied to Arabidopsis thaliana. Molecular plant-microbe interactions : MPMI 17: 696–706.
50. Gomez-GomezL, BollerT (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Molecular cell 5: 1003–1011.
51. LunaE, PastorV, RobertJ, FlorsV, Mauch-ManiB, et al. (2011) Callose deposition: a multifaceted plant defense response. Molecular plant-microbe interactions : MPMI 24: 183–193.
52. DelaneyTPUS, VernooijB, FriedrichL, WeymannK, NegrottoD, GaffneyT, Gut-RellaM, KessmannH, WardE, RyalsJ (1994) A central role of salicylic acid in plant disease resistance. Science 266: 1247–1250.
53. KlessigDF, DurnerJ, NoadR, NavarreDA, WendehenneD, et al. (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci U S A 97: 8849–8855.
54. KlessigDF, MalamyJ (1994) The salicylic acid signal in plants. Plant Mol Biol 26: 1439–1458.
55. EmansN, ZimmermannS, FischerR (2002) Uptake of a fluorescent marker in plant cells is sensitive to brefeldin A and wortmannin. The Plant cell 14: 71–86.
56. BolteS, TalbotC, BoutteY, CatriceO, ReadND, et al. (2004) FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. Journal of microscopy 214: 159–173.
57. JooS, LiuY, LuethA, ZhangS (2008) MAPK phosphorylation-induced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway. The Plant journal : for cell and molecular biology 54: 129–140.
58. WangH, LiuY, BruffettK, LeeJ, HauseG, et al. (2008) Haplo-insufficiency of MPK3 in MPK6 mutant background uncovers a novel function of these two MAPKs in Arabidopsis ovule development. Plant Cell 20: 602–613.
59. RasmussenMW, RouxM, PetersenM, MundyJ (2012) MAP Kinase Cascades in Arabidopsis Innate Immunity. Frontiers in plant science 3: 169.
60. HauckP, ThilmonyR, HeSY (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proceedings of the National Academy of Sciences of the United States of America 100: 8577–8582.
61. WangD, WeaverND, KesarwaniM, DongX (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308: 1036–1040.
62. NomuraK, DebroyS, LeeYH, PumplinN, JonesJ, et al. (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313: 220–223.
63. NomuraK, MeceyC, LeeYN, ImbodenLA, ChangJH, et al. (2011) Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 108: 10774–10779.
64. GuY, InnesRW (2012) The KEEP ON GOING protein of Arabidopsis regulates intracellular protein trafficking and is degraded during fungal infection. The Plant cell 24: 4717–4730.
65. JacobsAK, LipkaV, BurtonRA, PanstrugaR, StrizhovN, et al. (2003) An Arabidopsis Callose Synthase, GSL5, Is Required for Wound and Papillary Callose Formation. The Plant cell 15: 2503–2513.
66. NishimuraMT, SteinM, HouBH, VogelJP, EdwardsH, et al. (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301: 969–972.
67. KaldeM, NuhseTS, FindlayK, PeckSC (2007) The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proceedings of the National Academy of Sciences of the United States of America 104: 11850–11855.
68. DobrowolskiR, De RobertisEM (2012) Endocytic control of growth factor signalling: multivesicular bodies as signalling organelles. Nature reviews Molecular cell biology 13: 53–60.
69. ShiuSH, BleeckerAB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 2001: RE22.
70. MacGurnJA, HsuPC, EmrSD (2012) Ubiquitin and membrane protein turnover: from cradle to grave. Annual review of biochemistry 81: 231–259.
71. 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.
72. XuX, ChenC, FanB, ChenZ (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. The Plant cell 18: 1310–1326.
73. KimKC, LaiZ, FanB, ChenZ (2008) Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20: 2357–2371.
74. HuangJ, GuM, LaiZ, FanB, ShiK, et al. (2010) Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153: 1526–1538.
75. YangC-M, ChangK-W, YinM-H, HuangH-M (1998) Methods for determination of the chlorophylls and their derivatives. Taiwania 43: 116–122.
76. LaiZ, WangF, ZhengZ, FanB, ChenZ (2011) A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. The Plant journal : for cell and molecular biology 66: 953–968.
77. DietrichRA, DelaneyTP, UknesSJ, WardER, RyalsJA, et al. (1994) Arabidopsis mutants simulating disease resistance response. Cell 77: 565–577.
78. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743.
79. LaiZ, LiY, WangF, ChengY, FanB, et al. (2011) Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. The Plant cell 23: 3824–3841.
80. XieZ, FanB, ChenZ (1998) Induction of PR-1 proteins and potentiation of pathogen signals by salicylic acid exhibit the same dose response and structural specificity in plant cell cultures. Mol Plant-Microbe Interact 11: 568–571.
81. ChenZ, RiciglianoJW, KlessigDF (1993) Purification and characterization of a soluble salicylic acid-binding protein from tobacco. Proc Natl Acad Sci U S A 90: 9533–9537.
82. KimCY, LiuY, ThorneET, YangH, FukushigeH, et al. (2003) Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. The Plant cell 15: 2707–2718.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2014 Číslo 7
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Molecular and Cellular Mechanisms of KSHV Oncogenesis of Kaposi's Sarcoma Associated with HIV/AIDS
- Holobiont–Holobiont Interactions: Redefining Host–Parasite Interactions
- Helminth Infections, Type-2 Immune Response, and Metabolic Syndrome
- BCKDH: The Missing Link in Apicomplexan Mitochondrial Metabolism Is Required for Full Virulence of and