Skip to main content
SpringerLink
Log in

Vesicle Trafficking in Plant Pathogen Defence

  • Chapter
  • First Online:
Signaling in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Recent progress in our understanding of plant mechanisms has revealed important roles of vesicle trafficking in the cellular processes of pathogen defence. While most of the existing knowledge regarding the mechanistic details related to vesicle trafficking originates from non-plant systems, it is evident that most of these processes are also conserved in plants. Meanwhile, we are beginning to understand the general mechanisms of how plants and pathogens communicate and fight, and the present review summarises a collection of recent observations demonstrating how vesicle trafficking processes are linked to individual steps of this interaction. In this way, there is evidence showing that vesicle trafficking is involved both in regulating and in executing these defences. The vesicle-trafficking-related proteins documented to be associated with defence include syntaxins, soluble N-ethylmaleimide-sensitive factor attachment protein, vesicle-associated membrane protein dynamin, Rab GTPase, and a guanine nucleotide exchange factor of an ADP-ribosylation factor GTPase.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • An QL, Huckelhoven R, Kogel KH, van Bel AJE (2006) Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell Microbiol 8:1009–1019

    Article  PubMed  CAS  Google Scholar 

  • Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, Somerville CR, Thordal-Christensen H (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15:5118–5129

    Article  PubMed  CAS  Google Scholar 

  • Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, Parker JE (2006) Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 18:1038–1051

    Article  PubMed  CAS  Google Scholar 

  • Benschop JJ, Mohammed S, O'Flaherty M, Heck AJR, Slijper M, Menke FLH (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics 6:1198–1214

    Article  PubMed  CAS  Google Scholar 

  • Bonner MK, Skop AR (2008) Cell division screens and dynamin. Biochem Soc Trans 36:431–435

    Article  PubMed  CAS  Google Scholar 

  • Catanzariti AM, Dodds PN, Ellis JG (2007) Avirulence proteins from haustoria-forming pathogens. FEMS Microbiol Lett 269:181–188

    Article  PubMed  CAS  Google Scholar 

  • Cheon CI, Lee NG, Siddique ABM, Bal AK, Verma DPS (1993) Roles of plant homologs of Rab1P and Rab7P in the biogenesis of the peribacteroid membrane, a subcellular compartment formed de novo during root-nodule symbiosis. EMBO J 12:4125–4135

    PubMed  CAS  Google Scholar 

  • Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977

    Article  PubMed  CAS  Google Scholar 

  • de Wit PJGM (2007) How plants recognize pathogens and defend themselves. Cell Mol Life Sci 64:2726–2732

    Article  PubMed  CAS  Google Scholar 

  • Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847

    Article  PubMed  CAS  Google Scholar 

  • Douchkov D, Nowara D, Zierold U, Schweizer P (2005) A high-throughput gene-silencing system for the functional assessment of defense-related genes in barley epidermal cells. Mol Plant Microbe Interact 18:755–761

    Article  PubMed  CAS  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  PubMed  CAS  Google Scholar 

  • Edeling MA, Smith C, Owen D (2006) Life of a clathrin coat: insights from clathrin and AP structures. Nat Rev Mol Cell Biol 7:32–44

    Article  PubMed  CAS  Google Scholar 

  • Eichmann R, Huckelhoven R (2008) Accommodation of powdery mildew fungi in intact plant cells. J Plant Physiol 165:5–18

    Article  PubMed  CAS  Google Scholar 

  • Espinosa A, Alfano JR (2004) Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity. Cell Microbiol 6:1027–1040

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • Graham ME, Handley MTW, Barclay JW, Ciufo LF, Barrow SL, Morgan A, Burgoyne RD (2008) A gain-of-function mutant of Munc18–1 stimulates secretory granule recruitment and exocytosis and reveals a direct interaction of Munc18–1 with Rab3. Biochem J 409:407–416

    Article  PubMed  CAS  Google Scholar 

  • Hammond-Kosack KE, Parker JE (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193

    Article  PubMed  CAS  Google Scholar 

  • Hardham AR, Jones DA, Takemoto D (2007) Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol 10:342–348

    Article  PubMed  CAS  Google Scholar 

  • Heese A, Ludwig AA, Jones JD (2005) Rapid phosphorylation of a syntaxin during the Avr9/Cf-9-race-specific signaling pathway. Plant Physiol 138:2406–2416

    Article  PubMed  CAS  Google Scholar 

  • Heese M, Gansel X, Sticher L, Wick P, Grebe M, Granier F, Jurgens G (2001) Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J Cell Biol 155:239–249

    Article  PubMed  CAS  Google Scholar 

  • Hehnly H, Stamnes M (2007) Regulating cytoskeleton-based vesicle motility. FEBS Lett 581:2112–2118

    Article  PubMed  CAS  Google Scholar 

  • Hofius D, Tsitsigiannis DI, Jones JDG, Mundy J (2007) Inducible cell death in plant immunity. Semin Cancer Biol 17:166–187

    Article  PubMed  CAS  Google Scholar 

  • Ingmundson A, Delprato A, Lambright DG, Roy CR (2007) Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450:365–3U1

    Article  PubMed  CAS  Google Scholar 

  • Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15:2503–2513

    Article  PubMed  CAS  Google Scholar 

  • Jiang RHY, Tripathy S, Govers F, Tyler BM (2008) RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proc Natl Acad Sci U S A 105:4874–4879

    Article  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Kagan JC, Su T, Horng T, Chow A, Akira S, Medzhitov R (2008) TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat Immunol 9:361–368

    Article  PubMed  CAS  Google Scholar 

  • Kalde M, Nuhse TS, Findlay K, Peck SC (2007) The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc Natl Acad Sci U S A 104:11850–11855

    Article  PubMed  CAS  Google Scholar 

  • Kemen E, Kemen AC, Rafiqi M, Hempel U, Mendgen K, Hahn M, Voegele RT (2005) Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol Plant Microbe Interact 18:1130–1139

    Article  PubMed  CAS  Google Scholar 

  • Kirisits A, Pils D, Krainer M (2007) Epidermal growth factor receptor degradation: an alternative view of oncogenic pathways. Int J Biochem Cell Biol 39:2173–2182

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi Y, Kobayashi I, Funaki Y, Fujimoto S, Takemoto T, Kunoh H (1997) Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J 11:525–537

    Article  CAS  Google Scholar 

  • Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, El Kasmi F, Jurgens G, Parker J, Panstruga R, Lipka V, Schulze-Lefert P (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451:835–840

    Article  PubMed  CAS  Google Scholar 

  • Le Borgne R (2006) Regulation of Notch signalling by endocytosis and endosomal sorting. Curr Opin Cell Biol 18:213–222

    Article  PubMed  CAS  Google Scholar 

  • Leborgne-Castel N, Lherminier J, Der C, Fromentin J, Houot V, Simon-Plas F (2008) The plant defense elicitor cryptogein stimulates clathrin-mediated endocytosis correlated with reactive oxygen species production in bright yellow-2 tobacco cells. Plant Physiol 146:1255–1266

    Article  PubMed  CAS  Google Scholar 

  • Leyman B, Geelen D, Quintero FJ, Blatt MR (1999) A tobacco syntaxin with a role in hormonal control of guard cell ion channels. Science 283:537–540

    Article  PubMed  CAS  Google Scholar 

  • Lipka V, Kwon C, Panstruga R (2007) SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu Rev Cell Dev Biol 23:147–174

    Article  PubMed  CAS  Google Scholar 

  • Lorrain S, Vailleau F, Balague C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8:263–271

    Article  PubMed  CAS  Google Scholar 

  • Machner MP, Isberg RR (2007) A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 318:974–977

    Article  PubMed  CAS  Google Scholar 

  • Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J 29:257–268

    Article  PubMed  CAS  Google Scholar 

  • Miklis M, Consonni C, Bhat RA, Lipka V, Schulze-Lefert P, Panstruga R (2007) Barley MLO modulates actin-dependent and actin-independent antifungal defense pathways at the cell periphery. Plant Physiol 144:1132–1143

    Article  PubMed  CAS  Google Scholar 

  • Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972

    Article  PubMed  CAS  Google Scholar 

  • Nomura K, DebRoy S, Lee YH, Pumplin N, Jones J, He SY (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:220–223

    Article  PubMed  CAS  Google Scholar 

  • Nühse TS, Boller T, Peck SC (2003) A plasma membrane syntaxin is phosphorylated in response to the bacterial elicitor flagellin. J Biol Chem 278:45248–45254

    Article  PubMed  CAS  Google Scholar 

  • Opalski KS, Schultheiss H, Kogel KH, Huckelhoven R (2005) The receptor-like MLO protein and the RAC/ROP family G-protein RACB modulate actin reorganization in barley attacked by the biotrophic powdery mildew fungus Blumeria graminis f.sp hordei. Plant J 41:291–303

    Article  PubMed  CAS  Google Scholar 

  • Rehman RU, Stigliano E, Lycett GW, Sticher L, Sbano F, Faraco M, Dalessandro G, Di Sansebastiano GP (2008) Tomato Rab11a characterization evidenced a difference between SYP121-dependent and SYP122-dependent exocytosis. Plant Cell Physiol 49:751–766

    Article  PubMed  CAS  Google Scholar 

  • Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537–542

    Article  PubMed  CAS  Google Scholar 

  • Sanderfoot AA, Assaad FF, Raikhel NV (2000) The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. Plant Physiol 124:1558–1569

    Article  PubMed  CAS  Google Scholar 

  • Schiene K, Donath S, Brecht M, Puhler A, Niehaus K (2004) A Rab-related small GTP binding protein is predominantly expressed in root nodules of Medicago sativa. Mol Gen Genet 272:57–66

    CAS  Google Scholar 

  • Schultheiss H, Dechert C, Kogel KH, Huckelhoven R (2002) A small GTP-binding host protein is required for entry of powdery mildew fungus into epidermal cells of barley. Plant Physiol 128:1447–1454

    Article  PubMed  CAS  Google Scholar 

  • Schultheiss H, Dechert C, Kogel KH, Huckelhoven R (2003) Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus. Plant J 36:589–601

    Article  PubMed  CAS  Google Scholar 

  • Schultheiss H, Hensel G, Imani J, Broeders S, Sonnewald U, Kogel KH, Kumlehn J, Huckelhoven R (2005) Ectopic expression of constitutively activated RACB in barley enhances susceptibility to powdery mildew and abiotic stress. Plant Physiol 139:353–362

    Article  PubMed  CAS  Google Scholar 

  • Schultheiss H, Preuss J, Percher T, Eichmann R, Hückelhoven R (2008) Barley RIC171 interacts with RACB in planta and supports entry of the powdery mildew fungus. Cell Microbiol 10:1815–1826

    Article  PubMed  CAS  Google Scholar 

  • Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A (2007) Rab GTPases at a glance. J Cell Sci 120:3905–3910

    Article  PubMed  CAS  Google Scholar 

  • Shimada C, Lipka V, O'Connell R, Okuno T, Schulze-Lefert P, Takano Y (2006) Nonhost resistance in Arabidopsis-Colletotrichum interactions acts at the cell periphery and requires actin filament function. Mol Plant Microbe Interact 19:270–279

    Article  PubMed  CAS  Google Scholar 

  • Sokolovski S, Hills A, Gay RA, Blatt MR (2008) Functional interaction of the SNARE protein NtSyp121 in Ca2+ channel gating, Ca2+ transients and ABA signalling of stomatal guard cells. Mol Plant 1:347–358

    Article  PubMed  CAS  Google Scholar 

  • D'Souza-Schorey C, Chavrier P (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7:347–358

    Article  PubMed  CAS  Google Scholar 

  • Stark-Urnau M, Mendgen K (1995) Sequential deposition of plant glycoproteins and polysaccharides at the host-parasite interface of Uromyces vignae and Vigna sinensis - evidence for endocytosis and secretion. Protoplasma 186:1–11

    Article  CAS  Google Scholar 

  • Takemoto D, Jones DA, Hardham AR (2006) Re-organization of the cytoskeleton and endoplasmic reticulum in the Arabidopsis pen1–1 mutant inoculated with the non-adapted powdery mildew pathogen, Blumeria graminis f. sp hordei. Mol Plant Pathol 7:553–563

    Article  CAS  Google Scholar 

  • Tang D, Ade J, Frye CA, Innes RW (2006) A mutation in the GTP hydrolysis site of Arabidopsis dynamin-related protein 1E confers enhanced cell death in response to powdery mildew infection. Plant J 47:75–84

    Article  PubMed  CAS  Google Scholar 

  • Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J 46:34–53

    Article  PubMed  CAS  Google Scholar 

  • Truman W, de Zabala MT, Grant M (2006) Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J 46:14–33

    Article  PubMed  CAS  Google Scholar 

  • van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040

    Article  PubMed  CAS  Google Scholar 

  • Wei CF, Kvitko BH, Shimizu R, Crabill E, Alfano JR, Lin NC, Martin GB, Huang HC, Collmer A (2007) A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1–1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J 51:32–46

    Article  PubMed  CAS  Google Scholar 

  • Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S, Hein I, Toth IK, Pritchard L, Birch PRJ (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115–118

    Article  PubMed  CAS  Google Scholar 

  • Wienkoop S, Saalbach G (2003) Proteome analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiol 131:1080–1090

    Article  PubMed  CAS  Google Scholar 

  • Yun BW, Atkinson HA, Gaborit C, Greenland A, Read ND, Pallas JA, Loake GJ (2003) Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises non-host resistance in Arabidopsis against wheat powdery mildew. Plant J 34:768–777

    Article  PubMed  CAS  Google Scholar 

  • Zeyen RJ, Bushnell WR (1979) Papilla response of barley epidermal-cells caused by Erysiphe graminis – rate and method of deposition determined by microcinematography and transmission electron-microscopy. Can J Bot 57:898–913

    Article  Google Scholar 

  • Zhang Z, Feechan A, Pedersen C, Newman MA, Qiu JL, Olesen KL, Thordal-Christensen H (2007) A SNARE-protein has opposing functions in penetration resistance and defence signalling pathways. Plant J 49:302–312

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Lenk A, Andersson MX, Gjetting T, Pedersen C, Nielsen ME, Newman M-A, Hou B-H, Somerville SC, Thordal-Christensen H (2008) A lesion-mimic syntaxin double mutant in Arabidopsis reveals novel complexity of pathogen defense signaling. Mol Plant 1:510–527

    Article  PubMed  CAS  Google Scholar 

  • Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

I am grateful to Mads Eggert Nielsen, Carsten Pedersen, Dale Godfrey and Andrea Lenk for their critical reading of this manuscript.

Author information

Authors and Affiliations

  1. Plant and Soil Science Laboratory, Department of Agriculture and Ecology, The Royal Veterinary and Agricultural University, Thorvaldsensvej 40, Copenhagen, 1871, Frederiksberg C, Denmark

    Hans Thordal-Christensen*

Authors
  1. Hans Thordal-Christensen*
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

    Rights and permissions

    Reprints and permissions

    Copyright information

    © 2009 Springer-Verlag Berlin Heidelberg

    About this chapter

    Cite this chapter

    Thordal-Christensen*, H. (2009). Vesicle Trafficking in Plant Pathogen Defence. In: Mancuso, S., Balu¿ka, F. (eds) Signaling in Plants. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-89228-1_14

    Download citation

    Publish with us

    Policies and ethics

    Search

    Navigation