Skip to main content

The Role of the Plant Plasma Membrane in Microbial Sensing and Innate Immunity

  • Chapter
  • First Online:

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 19))

Abstract

Significant progress has recently been made in understanding the molecular mechanisms that determine plant immunity to microbial infection. Several plant plasma membrane pattern recognition receptors recognizing structurally diverse pathogen-derived molecular patterns pathogen-associated molecular patterns (PAMP) have been identified and shown to function in a similar manner as their counterparts mediating microbial pattern recognition and activation of innate immune defenses in animal systems. Receptor-mediated activation of immune response pathways results in the execution of plant defenses that in concert are supposed to halt microbial invasion. In turn, microbial infection strategies have evolved that aim at interfering with plant pattern recognition receptor function and, thus, highlight the importance of PAMP-triggered immunity in general and the important role of the plant plasma membrane as the contact interface between host and potential pathogen in particular.

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

Buying options

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

Learn about institutional subscriptions

References

  • Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42:385–414

    Article  PubMed  CAS  Google Scholar 

  • Aziz A, Gauthier A, Bezier A, Poinssot B, Joubert JM, Pugin A, Heyraud A, Baillieul F (2007) Elicitor and resistance-inducing activities of beta-1, 4 cellodextrins in grapevine, comparison with beta-1, 3 glucans and alpha-1, 4 oligogalacturonides. J Exp Bot 58:1463–1472

    Article  PubMed  CAS  Google Scholar 

  • Basse CW, Fath A, Boller T (1993) High affinity binding of a glycopeptide elicitor to tomato cells and microsomal membranes and displacement by specific glycan suppressors. J Biol Chem 268:14724–14731

    PubMed  CAS  Google Scholar 

  • Baureithel K, Felix G, Boller T (1994) Specific, high affinity binding of chitin fragments to tomato cells and membranes. J Biol Chem 269:17931–17938

    PubMed  CAS  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406

    Article  PubMed  CAS  Google Scholar 

  • Brunner F, Rosahl S, Lee J, Rudd JJ, Geiler S, Kauppinen S, Rasmussen G, Scheel D, Nürnberger T (2002) Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO J 21:6681–6688

    Article  PubMed  CAS  Google Scholar 

  • Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278:1963–1965

    Article  PubMed  CAS  Google Scholar 

  • Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500

    Article  PubMed  CAS  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  PubMed  CAS  Google Scholar 

  • Coaker G, Falick A, Staskawicz B (2005) Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308:548–550

    Article  PubMed  CAS  Google Scholar 

  • Darvill A, Bergmann C, Cervone F, De Lorenzo G, Ham KS, Spiro MD, York WS, Albersheim P (1994) Oligosaccharins involved in plant growth and host-pathogen interactions. Biochem Soc Symp 60:89–94

    PubMed  CAS  Google Scholar 

  • Erbs G, Silipo A, Aslam S, De Castro C, Liparoti V, Flagiello A, Pucci P, Lanzetta R, Parrilli M, Molinaro A, Newman MA, Cooper RM (2008) Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. Chem Biol 15:438–448

    Article  PubMed  CAS  Google Scholar 

  • Fauth M, Schweizer P, Buchala A, Markstadter C, Riederer M, Kato T, Kauss H (1998) Cutin monomers and surface wax constituents elicit H2O2 in conditioned cucumber hypocotyl segments and enhance the activity of other H2O2 elicitors. Plant Physiol 117:1373–1380

    Article  PubMed  CAS  Google Scholar 

  • Felix G, Grosskopf DG, Regenass M, Boller T (1991) Rapid changes of protein phosphorylation are involved in transduction of the elicitor signal in plant cells. Proc Natl Acad Sci USA 88:8831–8834

    Article  PubMed  CAS  Google Scholar 

  • Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–276

    Article  PubMed  CAS  Google Scholar 

  • Felix G, Boller T (2003) Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J Biol Chem 278:6201–6208

    Article  PubMed  CAS  Google Scholar 

  • Ferrandon D, Imler JL, Hetru C, Hoffmann JA (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7:862–874

    Article  PubMed  CAS  Google Scholar 

  • Gijzen M, Nürnberger T (2006) Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67:1800–1807

    Article  PubMed  CAS  Google Scholar 

  • Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP (2009) AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol 19:423–429

    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 

  • Godiard L, Sauviac L, Torii KU, Grenon O, Mangin B, Grimsley NH, Marco Y (2003) ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. Plant J 36:353–365

    Article  PubMed  CAS  Google Scholar 

  • Gohre V, Spallek T, Haweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield JW, Robatzek S (2008) Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol 18:1824–1832

    Article  PubMed  Google Scholar 

  • Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Gomez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7:251–256

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Gómez L, Bauer Z, Boller T (2001) Both the extracellular leucine rich repeat domain and the kinase activity of FLS2 are required for flagellin binding and signalling in Arabidopsis. Plant Cell 13:1155–1163

    PubMed  Google Scholar 

  • Granado J, Felix G, Boller T (1995) Perception of fungal sterols in plants. Plant Physiol 107:485–490

    PubMed  CAS  Google Scholar 

  • Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, Kemmerling B, Gotz F, Glawischnig E, Lee J, Felix G, Nurnberger T (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282:32338–32348

    Article  PubMed  CAS  Google Scholar 

  • Halim V, Hunger A, Macioszek V, Landgraf P, Nürnberger T, Scheel D, Rosahl S (2005) The oligopeptide elicitor Pep-13 induces salicylic acid-dependent and -independent defense reactions in potato. Physiol Mol Plant Pathol 64:311–318

    Article  Google Scholar 

  • Hauck P, Thilmony R, He SY (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci USA 100:8577–8582

    Article  PubMed  CAS  Google Scholar 

  • He SY, Huang HC, Collmer A (1993) Pseudomonas syringae pv. syringae harpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73:1255–1266

    Article  PubMed  CAS  Google Scholar 

  • He P, Shan L, Lin N-C, Martin G, Kemmerling B, Nürnberger T, Sheen J (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125:563–575

    Article  PubMed  CAS  Google Scholar 

  • He P, Shan L, Sheen J (2007) Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions. Cell Microbiol 9:1385–1396

    Article  PubMed  CAS  Google Scholar 

  • Ito Y, Kaku H, Shibuya N (1997) Identification of a high-affinity binding protein for N-acetylchitoologosaccharide elicitor in the plasma membrane of suspension-cultured rice cells by affinity labeling. Plant J 12:347–356

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103:11086–11091

    Article  PubMed  CAS  Google Scholar 

  • Kemmerling B, Schwedt A, Rodriguez P, Mazzotta S, Frank M, Qamar SA, Mengiste T, Betsuyaku S, Parker JE, Mussig C, Thomma BP, Albrecht C, de Vries SC, Hirt H, Nürnberger T (2007) The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Curr Biol 17:1116–1122

    Article  PubMed  CAS  Google Scholar 

  • Kim MG, da Cunha L, McFall AJ, Belkhadir Y, DebRoy S, Dangl JL, Mackey D (2005) Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121:749–759

    Article  PubMed  CAS  Google Scholar 

  • Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–3507

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Klessig DF, Nürnberger T (2001) A harpin binding site in tobacco plasma membranes mediates activation of the pathogenesis-related gene HIN1 independent of extracellular calcium but dependent on mitogen-activated protein kinase activity. Plant Cell 13:1079–1093

    PubMed  CAS  Google Scholar 

  • Li J, Wen J, Lease K, Doke J, Tax F, Walker J (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222

    Article  PubMed  CAS  Google Scholar 

  • Llorente F, Alonso-Blanco C, Sanchez-Rodriguez C, Jorda L, Molina A (2005) ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant J 43:165–180

    Article  PubMed  CAS  Google Scholar 

  • Mackey D, Holt BF III, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:1–20

    Article  Google Scholar 

  • Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–389

    Article  PubMed  CAS  Google Scholar 

  • Matzinger, P (2007) Friendly and dangerous signals: is the tissue in control? Nat Immunol 8:11–13

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449:819–826

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov R, Janeway C (1997) Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295–298

    Article  PubMed  CAS  Google Scholar 

  • Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980

    Article  PubMed  CAS  Google Scholar 

  • Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104:19613–19618

    Article  PubMed  CAS  Google Scholar 

  • Morillo SA, Tax FE (2006) Functional analysis of receptor-like kinases in monocots and dicots. Curr Opin Plant Biol 9:460–469

    Article  PubMed  CAS  Google Scholar 

  • Naito K, Taguchi F, Suzuki T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2008) Amino acid sequence of bacterial microbe-associated molecular pattern flg22 is required for virulence. Mol Plant Microbe Interact 21:1165–1174

    Article  PubMed  CAS  Google Scholar 

  • Newman MA, von Roepenack-Lahaye E, Parr A, Daniels MJ, Dow JM (2002) Prior exposure to lipopolysaccharide potentiates expression of plant defenses in response to bacteria. Plant J 29:487–495

    Article  PubMed  CAS  Google Scholar 

  • Nürnberger T, Kemmerling B (2006) Receptor protein kinases – pattern recognition receptors in plant immunity. Trends Plant Sci 11:519–522

    Article  PubMed  Google Scholar 

  • Nürnberger T, Lipka V (2005) Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6:335–345

    Article  PubMed  Google Scholar 

  • Nürnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K, Scheel D (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78:449–460

    Article  PubMed  Google Scholar 

  • Nürnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266

    Article  PubMed  Google Scholar 

  • Ottmann C, Luberacki B, Küfner I, Koch W, Brunner F, Weyand M, Mattinen L, Pirhonen M, Anderluh G, Seitz HU, Nürnberger T, Oecking C (2009) A common toxin fold mediates microbial attack and plant defense. Proc Natl Acad Sci USA 106(25):10359–10364

    Article  PubMed  CAS  Google Scholar 

  • Qutob D, Kemmerling B, Brunner F, Küfner I, Engelhardt S, Gust AA, Luberacki B, Seitz HU, Stahl D, Rauhut T, Glawischnig E, Schween G, Lacombe B, Watanabe N, Lam E, Schlichting R, Scheel D, Nau K, Dodt G, Hubert D, Gijzen M, Nürnberger T (2006) Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18:3721–3744

    Article  PubMed  CAS  Google Scholar 

  • Ron M, Avni A (2004) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604–1615

    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 

  • Seong SY, Matzinger P (2004) Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 4:469–478

    Article  PubMed  CAS  Google Scholar 

  • Shan L, He P, Li J, Heese A, Peck SC, Nürnberger T, Martin GB, Sheen J (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

    Article  PubMed  CAS  Google Scholar 

  • Van’t Slot K, Knogge W (2002) A dual role for microbial pathogen-derived effector proteins in plant disease and resistance. Crit Rev Plant Sci 21:229–271

    Article  Google Scholar 

  • Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9:203–209

    Article  PubMed  CAS  Google Scholar 

  • Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410:380–383

    Article  PubMed  CAS  Google Scholar 

  • Wang G, Ellendorff U, Kemp B, Mansfield JW, Forsyth A, Mitchell K, Bastas K, Liu CM, Woods-Tor A, Zipfel C, de Wit PJ, Jones JD, Tor M, Thomma BP (2008) A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol 147:503–517

    Article  PubMed  CAS  Google Scholar 

  • Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J, Zhou JM (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18:74–80

    Article  PubMed  CAS  Google Scholar 

  • Xing W, Zou Y, Liu Q, Liu J, Luo X, Huang Q, Chen S, Zhu L, Bi R, Hao Q, Wu JW, Zhou JM, Chai J (2007) The structural basis for activation of plant immunity by bacterial effector protein AvrPto. Nature 449:243–247

    Article  PubMed  CAS  Google Scholar 

  • Zipfel C, Felix G (2005) Plants and animals: a different taste for microbes? Curr Opin Plant Biol 8:353–360

    Article  PubMed  CAS  Google Scholar 

  • Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767

    Article  PubMed  CAS  Google Scholar 

  • Zipfel C, Kunze K, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the Arabidopsis receptor kinase EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Research in the lab of T.N. is supported by the Deutsche Forschungsgemeinschaft (AFGN, SFB 446, SFB 766, ERA-PG).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thorsten Nürnberger .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Nürnberger, T., Küfner, I. (2011). The Role of the Plant Plasma Membrane in Microbial Sensing and Innate Immunity. In: Murphy, A., Schulz, B., Peer, W. (eds) The Plant Plasma Membrane. Plant Cell Monographs, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-13431-9_22

Download citation

Publish with us

Policies and ethics