The Plasmodesmal Protein PDLP1 Localises to Haustoria-Associated Membranes during Downy Mildew Infection and Regulates Callose Deposition
Haustoria are specialised invasive structures that project from fungal or oomycete hyphae into host plant cells during infection, acting as sites for molecular exchange between host and pathogen. Haustoria are targets of plant defence responses, including the deposition of membranes and polysaccharides in an encasement structure that surrounds the haustorium. It is assumed that the encasement physically seals the haustorium off from the host cell. Here we have used cell biological and genetic approaches to reveal that the plasmodesmata-associated receptor-like protein PDLP1 plays a role in infection success of the Arabidopsis downy mildew pathogen, specifically in the development of the encasement. Using live cell imaging, we observed that PDLP1 relocates to the extra-haustorial membrane, and this is required for deposition of the polysaccharide callose in the encasement. This directly correlates pathogen success with the structure of the encasement, verifying the significance of the encasement in host defence. Further, our data pose the possibility that callose deposition at plasmodesmata and the haustorial encasement exploit similar mechanisms. Our findings shed light on plant defences at haustoria and how they inhibit pathogen success.
Vyšlo v časopise:
The Plasmodesmal Protein PDLP1 Localises to Haustoria-Associated Membranes during Downy Mildew Infection and Regulates Callose Deposition. PLoS Pathog 10(11): e32767. doi:10.1371/journal.ppat.1004496
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004496
Souhrn
Haustoria are specialised invasive structures that project from fungal or oomycete hyphae into host plant cells during infection, acting as sites for molecular exchange between host and pathogen. Haustoria are targets of plant defence responses, including the deposition of membranes and polysaccharides in an encasement structure that surrounds the haustorium. It is assumed that the encasement physically seals the haustorium off from the host cell. Here we have used cell biological and genetic approaches to reveal that the plasmodesmata-associated receptor-like protein PDLP1 plays a role in infection success of the Arabidopsis downy mildew pathogen, specifically in the development of the encasement. Using live cell imaging, we observed that PDLP1 relocates to the extra-haustorial membrane, and this is required for deposition of the polysaccharide callose in the encasement. This directly correlates pathogen success with the structure of the encasement, verifying the significance of the encasement in host defence. Further, our data pose the possibility that callose deposition at plasmodesmata and the haustorial encasement exploit similar mechanisms. Our findings shed light on plant defences at haustoria and how they inhibit pathogen success.
Zdroje
1. HahnM, MendgenK (2001) Signal and nutrient exchange at biotrophic plant-fungus interfaces. Curr Opin Plant Biol 4: 322–327.
2. MeyerD, PajonkS, MicaliC, O'ConnellR, Schulze-LefertP (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J 57: 986–999.
3. CaillaudMC, PiquerezSJ, FabroG, SteinbrennerJ, IshaqueN, et al. (2012) Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility. Plant J 69: 252–265.
4. LuYJ, SchornackS, SpallekT, GeldnerN, ChoryJ, et al. (2012) Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cell Microbiol 14: 682–697.
5. Harder DE, Chong J (1991) Rust Haustoria. In: Mendgen K, Lesemann D-E, editors. Electron microscopy of plant pathogens: Springer Berlin Heidelberg. pp.235–250.
6. KnaufGM, WelterK, MüllerM, MendgenK (1989) The haustorial host-parasite interface in rust-infected bean leaves after high-pressure freezing. Physiol Mol Plant Pathol 34: 519–530.
7. PerfectSE, GreenJR (2001) Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol 2: 101–108.
8. KohS, AndreA, EdwardsH, EhrhardtD, SomervilleS (2005) Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J 44: 516–529.
9. WangW, WenY, BerkeyR, XiaoS (2009) Specific targeting of the Arabidopsis resistance protein RPW8.2 to the interfacial membrane encasing the fungal haustorium renders broad-spectrum resistance to powdery mildew. Plant Cell 21: 2898–2913.
10. RobertsAM, MackieAJ, HathawayV, CallowJA, GreenJR (1993) Molecular differentiation in the extrahaustorial membrane of pea powdery mildew haustoria at early and late stages of development. Physiol Mol Plant Pathol 43: 147–160.
11. ChouCK (1970) An electron-microscope study of host penetration and early stages of haustorium formation of Peronospora parasitica (Fr.) tul. on cabbage cotyledons. Ann Bot 34: 189–204.
12. MimsCW, Rodriguez-LotherC, RichardsonEA (2002) Ultrastructure of the host-pathogen interface in daylily leaves infected by the rust fungus Puccinia hemerocallidis. Protoplasma 219: 221–226.
13. HeathMC (1976) Ultrastructural and functional similarity of the haustorial neckband of rust fungi and the Casparian strip of vascular plants. Can J Bot 54: 2484–2489.
14. Harder D E, J C (1984) Structure and physiology of haustoria. Bushnell W. R, Roelfs A. P, editors. Orlando, FL, USA: Academic Press, Inc, pp.431–476.
15. MimsCW, RichardsonEA, HoltBF3rd, DanglJL (2004) Ultrastructure of the host–pathogen interface in Arabidopsis thaliana leaves infected by the downy mildew Hyaloperonospora parasitica. Can J Bot 82: 1001–1008.
16. LunaE, PastorV, RobertJ, FlorsV, Mauch-ManiB, et al. (2011) Callose deposition: a multifaceted plant defense response. Mol Plant Microbe Interact 24: 183–193.
17. EulgemT, RushtonPJ, SchmelzerE, HahlbrockK, SomssichIE (1999) Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J 18: 4689–4699.
18. TonJ, FlorsV, Mauch-ManiB (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14: 310–317.
19. TorresMA, JonesJD, DanglJL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141: 373–378.
20. DongX, HongZ, ChatterjeeJ, KimS, VermaDP (2008) Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta 229: 87–98.
21. CaillaudMC, PiquerezSJ, JonesJD (2012) Characterization of the membrane-associated HaRxL17 Hpa effector candidate. Plant Signal Behav 7: 145–149.
22. FellbrichG, RomanskiA, VaretA, BlumeB, BrunnerF, et al. (2002) NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant Journal 32: 375–390.
23. SoyluEM, SoyluS (2003) Light and electron microscopy of the compatible interaction between Arabidopsis and the downy mildew pathogen Peronospora parasitica. J Phytopathol-Phytopathologische Zeitschrift 151: 300–306.
24. MicaliCO, NeumannU, GrunewaldD, PanstrugaR, O'ConnellR (2011) Biogenesis of a specialized plant-fungal interface during host cell internalization of Golovinomyces orontii haustoria. Cell Microbiol 13: 210–226.
25. DonofrioNM, DelaneyTP (2001) Abnormal callose response phenotype and hypersusceptibility to Peronospora parasitica in defense-compromised Arabidopsis nim1-1 and salicylate hydroxylase-expressing plants. Molecular Plant-Microbe Interactions 14: 439–450.
26. KeinathNF, KierszniowskaS, LorekJ, BourdaisG, KesslerSA, et al. (2010) PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J Biol Chem 285: 39140–39149.
27. StahlY, GrabowskiS, BleckmannA, KuhnemuthR, Weidtkamp-PetersS, et al. (2013) Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol 23: 362–371.
28. TilsnerJ, AmariK, TorranceL (2011) Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248: 39–60.
29. FaulknerC (2013) Receptor-mediated signaling at plasmodesmata. Front Plant Sci 4: 521.
30. RaffaeleS, BayerE, LafargeD, CluzetS, German RetanaS, et al. (2009) Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell 21: 1541–1555.
31. Fernandez-CalvinoL, FaulknerC, WalshawJ, SaalbachG, BayerE, et al. (2011) Arabidopsis plasmodesmal proteome. PLoS One 6: e18880.
32. MauleA, FaulknerC, Benitez-AlfonsoY (2012) Plasmodesmata "in Communicado". Front Plant Sci 3: 30.
33. ThomasCL, BayerEM, RitzenthalerC, Fernandez-CalvinoL, MauleAJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol 6: e7.
34. AmariK, BoutantE, HofmannC, Schmitt-KeichingerC, Fernandez-CalvinoL, et al. (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6: e1001119.
35. BayerE, ThomasC, MauleA (2008) Symplastic domains in the Arabidopsis shoot apical meristem correlate with PDLP1 expression patterns. Plant Signal Behav 3: 853–855.
36. LeeJY, WangX, CuiW, SagerR, ModlaS, et al. (2011) A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23: 3353–3373.
37. ZavalievR, UekiS, EpelBL, CitovskyV (2011) Biology of callose (beta-1,3-glucan) turnover at plasmodesmata. Protoplasma 248: 117–130.
38. BricchiI, OcchipintiA, BerteaCM, ZebeloSA, BrilladaC, et al. (2013) Separation of early and late responses to herbivory in Arabidopsis by changing plasmodesmal function. Plant J 73: 14–25.
39. AsaiS, PiquerezSJM, RallapalliaG, CaillaudMC, FurzerO, et al. (2014) Expression profiling during Arabidopsis/downy mildew interaction uncovers a highly-expressed effector which reduces salicylic acid-triggered immunity. PLoS Pathogens 10: e1004443 DOI:10.1371/journal.ppat.1004443
40. VogelF, HofiusD, SonnewaldU (2007) Intracellular trafficking of potato leafroll virus movement protein in transgenic Arabidopsis. Traffic 8: 1205–1214.
41. SimpsonC, ThomasC, FindlayK, BayerE, MauleAJ (2009) An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21: 581–594.
42. van der BiezenEA, FreddieCT, KahnK, ParkerJE, JonesJD (2002) Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components. Plant J 29: 439–451.
43. MukhtarMS, CarvunisAR, DrezeM, EppleP, SteinbrennerJ, et al. (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333: 596–601.
44. SteinM, DittgenJ, Sanchez-RodriguezC, HouBH, MolinaA, et al. (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18: 731–746.
45. CollinsNC, Thordal-ChristensenH, LipkaV, BauS, KombrinkE, et al. (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425: 973–977.
46. KohornBD, KohornSL, TodorovaT, BaptisteG, StanskyK, et al. (2012) A dominant allele of Arabidopsis pectin-binding wall-associated kinase induces a stress response suppressed by MPK6 but not MPK3 mutations. Mol Plant 5: 841–851.
47. LiuJ, ElmoreJM, FuglsangAT, PalmgrenMG, StaskawiczBJ, et al. (2009) RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol 7: e1000139.
48. KimH, O'ConnellR, Maekawa-YoshikawaM, UemuraT, NeumannU, et al. (2014) The powdery mildew resistance protein RPW8.2 is carried on VAMP721/722 vesicles to the extrahaustorial membrane of haustorial complexes. Plant J 79: 835–847 DOI: 10.1111/tpj.12591
49. KwonC, NeuC, PajonkS, YunHS, LipkaU, et al. (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451: 835–840.
50. NagasakiN, TomiokaR, MaeshimaM (2008) A hydrophilic cation-binding protein of Arabidopsis thaliana, AtPCaP1, is localized to plasma membrane via N-myristoylation and interacts with calmodulin and the phosphatidylinositol phosphates PtdIns(3,4,5)P(3) and PtdIns(3,5)P(2). FEBS J 275: 2267–2282.
51. CarmanGM, HanGS (2006) Roles of phosphatidate phosphatase enzymes in lipid metabolism. Trends Biochem Sci 31: 694–699.
52. PetermanTK, OholYM, McReynoldsLJ, LunaEJ (2004) Patellin1, a novel Sec14-like protein, localizes to the cell plate and binds phosphoinositides. Plant Physiol 136: 3080–3094 discussion 3001–3082.
53. El KasmiF, KrauseC, HillerU, StierhofYD, MayerU, et al. (2013) SNARE complexes of different composition jointly mediate membrane fusion in Arabidopsis cytokinesis. Mol Biol Cell 24: 1593–1601.
54. ZhangL, ZhangH, LiuP, HaoH, JinJB, et al. (2011) Arabidopsis R-SNARE proteins VAMP721 and VAMP722 are required for cell plate formation. PLoS One 6: e26129.
55. VogelJ, SomervilleS (2000) Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc Natl Acad Sci U S A 97: 1897–1902.
56. ZhouJ, SpallekT, FaulknerC, RobatzekS (2012) CalloseMeasurer: a novel software solution to measure callose deposition and recognise spreading callose patterns. Plant Methods 8: 49.
57. BakaZA (2008) Occurrence and ultrastructure of Albugo candida on a new host, Arabis alpina in Saudi Arabia. Micron 39: 1138–1144.
58. Benitez-AlfonsoY, FaulknerC, PendleA, MiyashimaS, HelariuttaY, et al. (2013) Symplastic intercellular connectivity regulates lateral root patterning. Dev Cell 26: 136–147.
59. GusemanJM, LeeJS, BogenschutzNL, PetersonKM, VirataRE, et al. (2010) Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis chorus (glucan synthase-like 8). Development 137: 1731–1741.
60. HahnM, NeefU, StruckC, GottfertM, MendgenK (1997) A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. Mol Plant-Microbe Interact 10: 438–445.
61. VoegeleRT, StruckC, HahnM, MendgenK (2001) The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci USA 98: 8133–8138.
62. VoegeleRT, WirselS, MollU, LechnerM, MendgenK (2006) Cloning and characterization of a novel invertase from the obligate biotroph Uromyces fabae and analysis of expression patterns of host and pathogen invertases in the course of infection. Mol Plant-Microbe Interact 19: 625–634.
63. StruckC, HahnM, MendgenK (1996) Plasma membrane H+-ATPase activity in spores, germ tubes, and haustoria of the rust fungus Uromyces viciae-fabae. Fungal Gen Biol 20: 30–35.
64. StruckC, SiebelsC, RommelO, WernitzM, HahnM (1998) The plasma membrane H+-ATPase from the biotrophic rust fungus Uromyces fabae: Molecular characterization of the gene (PMA1) and functional expression of the enzyme in yeast. Mol Plant-Microbe Interact 11: 458–465.
65. CatanzaritiAM, DoddsPN, EllisJG (2007) Avirulence proteins from haustoria-forming pathogens. FEMS Microbiol Lett 269: 181–188.
66. DoddsPN, RafiqiM, GanPH, HardhamAR, JonesDA, et al. (2009) Effectors of biotrophic fungi and oomycetes: pathogenicity factors and triggers of host resistance. New Phytol 183: 993–1000.
67. LinkTI, VoegeleRT (2008) Secreted proteins of Uromyces fabae: similarities and stage specificity. Mol Plant Pathol 9: 59–66.
68. WhissonSC, BoevinkPC, MolelekiL, AvrovaAO, MoralesJG, et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450: 115–118.
69. BozkurtTO, SchornackS, WinJ, ShindoT, IlyasM, et al. (2011) Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc Natl Acad Sci U S A 108: 20832–20837.
70. ZhangH, WangC, ChengY, ChenX, HanQ, et al. (2012) Histological and cytological characterization of adult plant resistance to wheat stripe rust. Plant Cell Rep 31: 2121–2137.
71. ZhangH, WangC, ChengY, WangX, LiF, et al. (2011) Histological and molecular studies of the non-host interaction between wheat and Uromyces fabae. Planta 234: 979–991.
72. JacobsAK, LipkaV, BurtonRA, PanstrugaR, StrizhovN, et al. (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15: 2503–2513.
73. NishimuraMT, SteinM, HouBH, VogelJP, EdwardsH, et al. (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301: 969–972.
74. AndersonRG, CasadyMS, FeeRA, VaughanMM, DebD, et al. (2012) Homologous RXLR effectors from Hyaloperonospora arabidopsidis and Phytophthora sojae suppress immunity in distantly related plants. Plant J 72: 882–893.
75. CaillaudMC, AsaiS, RallapalliG, PiquerezS, FabroG, et al. (2013) A downy mildew effector attenuates salicylic acid-triggered immunity in Arabidopsis by interacting with the host mediator complex. PLoS Biol 11: e1001732.
76. Chong J, Harder (1982) Ultrastructure of haustorium development in Puccinia coronata avenae: some host responses. Phytopathology: 1527–1533.
77. KarimiM, InzeD, DepickerA (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193–195.
78. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743.
79. Robert-SeilaniantzA, MacleanD, JikumaruY, HillL, YamaguchiS, et al. (2011) The microRNA miR393 redirects secondary metabolite biosynthesis away from camalexin and towards glucosinolates. Plant J 67: 218–31.
80. ThistlethwaiteP, PorterI, EvansN (1986) Photophysics of the aniline blue fluorophore - a fluorescent-probe showing specificity toward (1-]3)-beta-D-glucans. J Phys Chem 90: 5058–5063.
81. WellsB (1985) Low temperature box and tissue handling device for embedding biological tissue for immunostaining in electron microscopy. Micron and Microscopica Acta 16: 49–53.
82. SearleBC (2010) Scaffold: a bioinformatic tool for validating MS/MS-based proteomic studies. Proteomics 10: 1265–1269.
83. KellerA, NesvizhskiiAI, KolkerE, AebersoldR (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383–5392.
84. NesvizhskiiAI, KellerA, KolkerE, AebersoldR (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646–4658.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2014 Číslo 11
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Coronavirus Cell Entry Occurs through the Endo-/Lysosomal Pathway in a Proteolysis-Dependent Manner
- War and Infectious Diseases: Challenges of the Syrian Civil War
- The Epithelial αvβ3-Integrin Boosts the MYD88-Dependent TLR2 Signaling in Response to Viral and Bacterial Components
- Peculiarities of Prion Diseases