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Experimental Evidence of a Role for RLKs in Innate Immunity

  • Thomas BollerEmail author
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 13)

Abstract

Four lines of experimental evidence point to a major role of RLKs in plant innate immunity. First, several RLKs are located at the plasma membrane and perceive specific “microbe-associated molecular patterns” (MAMPs), such as bacterial flagellin, bacterial EF-Tu or fungal chitin. The high affinity and specificity of these RLKs for their respective ligands, and the absence of endogenous ligands in plants, strongly indicate that these RLKs serve as “pattern recognition receptors” (PRRs) to signal the presence of microbes. Second, mutational loss of individual PRRs can lead to a reduced resistance against pathogens. Third, biotechnological transfer of a PRR from one given plant species to another may lead to increased resistance against pathogens. Fourth, and most importantly, successful pathogens produce effectors that inhibit the PRRs themselves or prevent the signal transduction pathways activated upon stimulation of the PRRs.

Keywords

Perception System Avirulence Gene Innate Immunity Receptor Induce Defense Response Nanomolar Level 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nature Rev Mol Cell Biol 7:601–611CrossRefGoogle Scholar
  2. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511PubMedCrossRefGoogle Scholar
  3. Albert M, Jehle AK, Lipschis M, Mueller K, Zeng Y, Felix G (2010) Regulation of cell behaviour by plant receptor kinases: pattern recognition receptors as prototypical models. Eur J Cell Biol 89:200–207PubMedCrossRefGoogle Scholar
  4. Andersen-Nissen E, Smith KD, Strobe KL, Barrett SLR, Cookson BT, Logan SM, Aderem A (2005) Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci USA 102:9247–9252PubMedCrossRefGoogle Scholar
  5. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gómez-Gómez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983PubMedCrossRefGoogle Scholar
  6. Boller T (1995) Chemoperception of microbial signals in plant cells. Ann Rev Plant Physiol Plant Mol Biol 46:189–214CrossRefGoogle Scholar
  7. Boller T (2008) Stabbing in the BAK – an original target for avirulence genes of plant pathogens. Cell Host Microbe 4:5–7PubMedCrossRefGoogle Scholar
  8. 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 60:379–406PubMedCrossRefGoogle Scholar
  9. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744PubMedCrossRefGoogle Scholar
  10. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500PubMedCrossRefGoogle Scholar
  11. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814PubMedCrossRefGoogle Scholar
  12. Collier SM, Moffett P (2009) NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci 14:521–529PubMedCrossRefGoogle Scholar
  13. Cui HT, Xiang TT, Zhou JM (2009) Plant immunity: a lesson from pathogenic bacterial effector proteins. Cell Microbiol 11:1453–1461PubMedCrossRefGoogle Scholar
  14. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  15. Darvill AG, Albersheim P (1984) Phytoalexins and their elicitors – a defense against microbial infection in plants. Ann Rev Plant Physiol Plant Mol Biol 35:243–275CrossRefGoogle Scholar
  16. Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JDG (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451–459PubMedCrossRefGoogle Scholar
  17. Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284PubMedCrossRefGoogle Scholar
  18. Espinosa A, Alfano JR (2004) Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity. Cell Microbiol 6:1027–1040PubMedCrossRefGoogle Scholar
  19. 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 278:6201–6208PubMedCrossRefGoogle Scholar
  20. Felix G, Regenass M, Boller T (1993) Specific perception of subnanomolar concentrations of chitin fragments by tomato cells – induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J 4:307–316CrossRefGoogle Scholar
  21. 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 18:265–276PubMedCrossRefGoogle Scholar
  22. Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011PubMedCrossRefGoogle Scholar
  23. Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18:277–284PubMedCrossRefGoogle Scholar
  24. Hamel LP, Beaudoin N (2011) Chitooligosaccharide sensing and downstream signaling: contrasted outcomes in pathogenic and beneficial plant-microbe interactions. Planta 232:787–806CrossRefGoogle Scholar
  25. 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 100:8577–8582PubMedCrossRefGoogle Scholar
  26. Hayashi F, Smith KD, Ozinsky A et al (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099–1103PubMedCrossRefGoogle Scholar
  27. Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217–12222PubMedCrossRefGoogle Scholar
  28. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  29. Jones DA, Thomas CM, Hammond-Kosack KE, Balintkurti PJ, Jones JDG (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793PubMedCrossRefGoogle Scholar
  30. Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Ann Rev Genet 24:447–463PubMedCrossRefGoogle Scholar
  31. Kim YJ, Lin NC, Martin GB (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589–598PubMedCrossRefGoogle Scholar
  32. 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 16:3496–3507PubMedCrossRefGoogle Scholar
  33. Lacombe S, Rougon-Cardoso A, Sherwood E et al (2010) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol 28:365–369PubMedCrossRefGoogle Scholar
  34. Lehti-Shiu MD, Zou C, Hanada K, Shiu SH (2009) Evolutionary history and stress regulation of plant receptor-like kinase/Pelle genes. Plant Physiol 150:12–26PubMedCrossRefGoogle Scholar
  35. Lin NC, Martin GB (2005) An avrPto/avrPtoB mutant of Pseudomonas syringae pv. tomato DC3000 does not elicit Pto-mediated resistance and is less virulent on tomato. Mol Plant-Microbe Interact 18:43–51PubMedCrossRefGoogle Scholar
  36. Mackey D, McFall AJ (2006) MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol Microbiol 61:1365–1371PubMedCrossRefGoogle Scholar
  37. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedCrossRefGoogle Scholar
  38. Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46:101–122PubMedCrossRefGoogle Scholar
  39. Müller K, Felix G (2011) Ligands of RLKs and RLPs involved in defense and symbiosis. In: Tax F, Kemmerling B (eds) Receptor-like kinases in plants. Springer, HeidelbergGoogle Scholar
  40. Nürnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K, Scheel D (1994) High affinity binding of a binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78:449–460PubMedCrossRefGoogle Scholar
  41. Park CJ, Han SW, Chen XW, Ronald PC (2010) Elucidation of Xa21-mediated innate immunity. Cell Microbiol 12:1017–1025PubMedCrossRefGoogle Scholar
  42. Pfund C, Tans-Kersten J, Dunning FM, Alonso JM, Ecker JR, Allen C, Bent AF (2004) Flagellin is not a major defense elicitor in Ralstonia solanacearum cells or extracts applied to Arabidopsis thaliana. Mol Plant-Microbe Interact 17:696–706PubMedCrossRefGoogle Scholar
  43. Robatzek S, Bittel P, Chinchilla D, Köchner P, Felix GS, Boller HST (2007) Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol Biol 64:539–547PubMedCrossRefGoogle Scholar
  44. Ronald PC, Beutler B (2010) Plant and animal sensors of conserved microbial signatures. Science 330:1061–1064PubMedCrossRefGoogle Scholar
  45. Schulze B, Mentzel T, Jehle AK, Mueller K, Beeler S, Boller T, Felix G, Chinchilla D (2010) Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem 285:9444–9451PubMedCrossRefGoogle Scholar
  46. Segonzac C, Zipfel C (2011) Activation of plant pattern-recognition receptors by bacteria. Curr Opin Microbiol 14:54–61PubMedCrossRefGoogle Scholar
  47. Shan L, He P, Li J, Heese A, Peck SC, Nürnberger T, Martin GB, Sheen J (2008) Bacterial effectors target BAK1 to disrupt MAMP receptor signaling complexes and impede plant innate immunity. Cell Host Microbe 4:17–27PubMedCrossRefGoogle Scholar
  48. Song WY, Wang GL, Chen LL et al (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806PubMedCrossRefGoogle Scholar
  49. Staskawicz BJ, Dahlbeck D, Keen NT (1984) Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibilty on Glycine max (L) Merr. Proc Natl Acad Sci USA 81:6024–6028PubMedCrossRefGoogle Scholar
  50. Sun WX, Dunning FM, Pfund C, Weingarten R, Bent AF (2006) Within-species flagellin polymorphism in Xanthomonas campestris pv. campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses. Plant Cell 18:764–779PubMedCrossRefGoogle Scholar
  51. Xiang T, Zong N, Zou Y et al (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18:74–80PubMedCrossRefGoogle Scholar
  52. Xiang TT, Zong N, Zhang J, Chen JF, Chen MS, Zhou JM (2011) BAK1 Is not a target of the Pseudomonas syringae effector AvrPto. Mol Plant-Microbe Interact 24:100–107PubMedCrossRefGoogle Scholar
  53. Zeng WQ, He SY (2010) A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol 153:1188–1198PubMedCrossRefGoogle Scholar
  54. Zhang J, Shao F, Cui H et al (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1:175–185PubMedCrossRefGoogle Scholar
  55. Zipfel C, Robatzek S (2010) Pathogen-associated molecular pattern-triggered immunity: Veni, vidi … ? Plant Physiol 154:551–554PubMedCrossRefGoogle Scholar
  56. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767PubMedCrossRefGoogle Scholar
  57. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Zürich-Basel Plant Science Center, Botanical InstituteUniversity BaselBaselSwitzerland

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