Suppression of Plant Defences by Nematodes



Biotrophic plant parasites rely on a single feeding site for all the nutrients required throughout their life cycle and these feeding structures therefore have to be kept alive for a period of up to six weeks. However, plants have well developed systems for detection of biotrophic pathogens and destruction of the pathogen or the plant tissues on which they depend. The mechanisms used by plant nematodes to protect themselves from direct attack by their hosts are relatively well characterised and show many parallels to the systems employed by animal parasitic nematodes to protect themselves from the immune responses of their hosts. In both cases housekeeping antioxidant proteins become changed in their expression patterns so that they are present at the host-parasite interface where they can detoxify host derived active oxygen species in a fine example of convergent evolution. However, the systems by which plant nematodes protect their biotrophic feeding structures are less well characterised. The available evidence to date suggests parallels with other plant pathogenic micro-organisms.


Biotrophy PAMP-Triggered immunity Effector-Triggered immunity Host defences 


  1. Armstrong MR, Whisson SC, Pritchard L, Bos JIB, Venter E, Avrova AO, Rehmany AP, Bohme U, Brooks K, Cheravach I, Hamlin N, White B, Fraser A, Lord A, Quail MA, Churcher C, Hall N, Berriman M, Huang S, Kamoun S, Birch PRJ (2005) An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc Nat Acad Sci U S A 102:7766–7771CrossRefGoogle Scholar
  2. Balic A, Harcus Y, Holland MJ, Maizels RM (2004) Selective maturation of dendritic cells by Nippostrongylus brasiliensis secreted proteins drives Th2 immune responses. Eur J Immunol 34:3047–3059PubMedCrossRefGoogle Scholar
  3. Bent AF, Mackey D (2008) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Ann Rev Phytopathol 45:399–436CrossRefGoogle Scholar
  4. Bos JIB, Kanneganti T-D, Young C, Cakir C, Huitema E, Win J, Armstrong MR, Birch PRJ, Kamoun S (2006) The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a mediated hypersensitivity and suppress INF1—induced cell death in Nicotiana benthamiana. Plant J 48:165–176PubMedCrossRefGoogle Scholar
  5. Campbell AM, Teesdale-Spittle PH, Barrett J, Liebau E, Jeffries JR, Brophy PM (2001) A common class of nematode glutathione S transferase (GST) revealed by the theoretical proteome fo the model organism Caenorhabditis elegans. Comp Biochem Physiolt B Biochem Mol Biol 128:701–708CrossRefGoogle Scholar
  6. Casteel CL, Walling LL, Paine TD (2006) Behaviour and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi-1.2 gene. Entomol Experimentalis App 121:67–72CrossRefGoogle Scholar
  7. 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
  8. Craig A, Ewan R, Mesmar J, Gudipati V, Sadanandom A (2009) E3 ubiquitin ligases and plant innate immunity. J Exp Bot 60:1123–1132PubMedCrossRefGoogle Scholar
  9. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  10. De Jonge R, Thomma BPHJ (2009) Fungal LysM effectors: extinguishers of host immunity? Trends Microbiol 17:151–157PubMedCrossRefGoogle Scholar
  11. Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, De Lorenzo G, Ferrari S, Ausubel FM, Dewdney J (2008) Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol Plant 1:423–445PubMedCrossRefGoogle Scholar
  12. De Veer MJ, Kemp JM, Meeusen ENT (2007) The innate host defence against nematode parasites. Parasite Immunol 29:1–9PubMedCrossRefGoogle Scholar
  13. Dixon MS, Golstein C, Thomas CM, van der Biezen EA, Jones JDG (2000) Genetic complexity of pathogen perception by plants: The example of Rcr3, a tomato gene required specifically by Cf-2. Proc Nat Acad Sci U S A 97:8807–8814CrossRefGoogle Scholar
  14. Dubreuil G, Magliano M, Deleury E, Abad P, Rosso MN (2007) Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism. New Phytol 176:426–436PubMedCrossRefGoogle Scholar
  15. Ellis JG, Rafiqi M, Gan P, Chakrabarti A, Dodds PN (2009) Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens. Curr Opin Plant Biol 12:399–405PubMedCrossRefGoogle Scholar
  16. Garofalo A, Kennedy MW, Bradley JE (2003a) The FAR proteins of parasitic nematodes: their possible involvement in the pathogenesis of infection and the use of Caenorhabditis elegans as a model system to evaluate their function. Med Microbiol Immunol 192:47–52Google Scholar
  17. Garofalo A, Rowlinson MC, Amambua NA, Hughes JM, Kelly SM, Price NC, Cooper A, Watson DG, Kennedy MW, Bradley JE (2003b) The FAR protein family of the nematode Caenorhabditis elegans—Differential lipid binding properties, structural characteristics, and developmental regulation. J Biol Chem 278:8065–8074CrossRefGoogle Scholar
  18. Ghosh I, Eisinger SW, Raghavan N, Scott AL (1998) Thioredoxin peroxidases from Brugia malayi. Mol Biochem Parasit 91:207–220CrossRefGoogle Scholar
  19. Gleason CA, Liu QL, Williamson VM (2008) Silencing a candidate nematode effector gene corresponding to the tomato resistance gene Mi-1 leads to acquisition of virulence. Mol Plant-Mic Interact 21:576–585CrossRefGoogle Scholar
  20. Göhre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Ann Rev Phytopathol 46:189–215CrossRefGoogle Scholar
  21. Göhre V, Spallek T, Häweker 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 18:1824–1832PubMedCrossRefGoogle Scholar
  22. Golinowski W, Sobczak M, Kurek W, Grymaszewska G (1997) The structure of syncytia. In: Fenoll C, Grundler FMW, Ohl S (eds) Cellular and molecular aspects of plant-nematode interactions. Kluwer Academic, Dordrecht, pp 80–97CrossRefGoogle Scholar
  23. Grundler FMW, Sobczak M, Lange S (1997) Defence responses of Arabidopsis thaliana during invasion and feeding site induction by the plant-parasitic nematode Heterodera glycines. Physiol Mol Plant Pathol 50:419–429CrossRefGoogle Scholar
  24. Hann DR, Rathjen JP (2007) Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J 49:607–618PubMedCrossRefGoogle Scholar
  25. Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, Bozkurt TO, Ah-Fong AMV, Alvarado L, Anderson VL, Armstrong MR, Avrova A, Baxter L, Beynon J, Boevink PC, Bollmann SR, Bos JIB, Bulone V, Cai G, Cakir C, Carrington JC, Chawner M, Conti L, Costanzo S, Ewan R, Fahlgren N, Fischbach MA, Fugelstad J, Gilroy EM, Gnerre S, Green PJ, Grenville-Briggs LJ, Griffith J, Grünwald NJ, Horn K, Horner NR, Hu C.-H, Huitema E, Jeong D.-H, Jones AME, Jones JDG, Jones RW, Karlsson EK, Kunjeti SG, Lamour K, Liu Z, Ma L, MacLean D, Chibucos MC, McDonald H, McWalters J, Meijer HJG, Morgan W, Morris PF, Munro CA, O’Neill K, Ospina-Giraldo M, Pinzón A, Pritchard L, Ramsahoye B, Ren Q, Restrepo S, Roy S, Sadanandom A, Savidor A, Schornack S, Schwartz DC, Schumann UD, Schwessinger B, Seyer L, Sharpe T, Silvar C, Song J, Studholme DJ, Sykes S, Thines M, Van De Vondervoort PJI, Phuntumart V, Wawra S, Weide R, Win J, Young C, Zhou S, Fry W, Meyers BC, Van West P, Ristaino J, Govers F, Birch PRJ, Whisson SC, Judelson HS, Nusbaum C (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nat 461:393–398Google Scholar
  26. Henkle-Duhrsen K, Kampkotter A (2001) Antioxidant enzyme families in parasitic nematodes. Mol Biochem Parasitol 114:129–142PubMedCrossRefGoogle Scholar
  27. Hein I, Gilroy EM, Armstrong MR, Birch PRJ (2009) The zig-zag-zig in oomycete-plant interactions. Mol Plant Pathol 10:547–562PubMedCrossRefGoogle Scholar
  28. Jasmer DP, Goverse A, Smant G (2003) Parasitic nematode interactions with animals and plants. Ann Rev Phytopathol 41:245–270CrossRefGoogle Scholar
  29. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19:4004–4014PubMedCrossRefGoogle Scholar
  30. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  31. Jones JT, Reavy B, Smant G, Prior AE (2004) Glutathione peroxidases of the potato cyst nematode Globodera rostochiensis. Gene 324:47–54PubMedCrossRefGoogle Scholar
  32. Kamoun S, Hamada W, Huitema E (2003) Agrosuppression: a bioassay for the hypersensitive response suited to highthroughput screening. Mol Plant-Micr Interact 16:7–13CrossRefGoogle Scholar
  33. Kay S, Bonas U (2009) How Xanthomonas type III effectors manipulate the host plant. Curr Opin Microbiol 12:37–43PubMedCrossRefGoogle Scholar
  34. Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:648–651PubMedCrossRefGoogle Scholar
  35. 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
  36. Kim MG, Da Cunha L, McFall AJ, Belkhadir Y, DebRoy S, Dangl JL, Mackey D (2005a) Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121:749–759CrossRefGoogle Scholar
  37. Kim HS, Desveaux D, Singer AU, Patel P, Sondek J, Dangl JL (2005b) The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc Nat Acad Sci USA 102:6496–6501CrossRefGoogle Scholar
  38. Klimowski L, Chandrashekar R, Tripp CA (1997) Molecular cloning, expression and enzymatic activity of a thioredoxin peroxidase from Dirofilaria immitis. Mol Biochem Parasitol 90:297–306PubMedCrossRefGoogle Scholar
  39. Libault M, Wan J, Czechowski T, Udvardi M, Stacey G (2007) Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol Plant-Mic Interact 20:900–911CrossRefGoogle Scholar
  40. Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn NR, DeVera, ME, Liang X, Tör M, Billiar T (2007) The grateful dead: Damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 220:60–81PubMedCrossRefGoogle Scholar
  41. Lu WH, Egerton GL, Bianco AE, Williams SA (1998) Thioredoxin peroxidase from Onchocerca volvulus: a major hydrogen peroxide detoxifying enzyme in filarial parasites. Mol Biochem Parasitol 91:221–235PubMedCrossRefGoogle Scholar
  42. Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–754PubMedCrossRefGoogle Scholar
  43. Mur LAJ, Kenton P, Lloyd AJ, Ougham H, Prats E (2008) The hypersensitive response; The centenary is upon us but how much do we know? J Exp Bot 59:501–520PubMedCrossRefGoogle Scholar
  44. Nombela G, Williamson VM, Muñiz M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol Plant-Mic Interact 16:645–649CrossRefGoogle Scholar
  45. Nurnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266PubMedCrossRefGoogle Scholar
  46. Paulson RE, Webster JM (1972) Ultrastructure of the hypersensitive reaction in roots of tomato, Lycopersicon esculentum L., to infection by the root-knot nematode, Meloidogyne incognita. Physiol Plant Pathol 2:227–230CrossRefGoogle Scholar
  47. Prins TW, Wagemakers L, Schouten A, van Kan JAL (2001) Cloning and characterization of a glutathione s-transferase homologue from the plant pathogenic fungus Botrytis cinerea. Mol Plant Pathol 1:169–178CrossRefGoogle Scholar
  48. Prior AE, Jones JT, Blok VC, Beauchamp J, McDermott L, Cooper A, Kennedy MW (2001) A surface-associated retinol- and fatty acid-binding protein (GpLBP20) from the potato cyst nematode Globodera pallida—lipid binding activities, structural analysis and expression pattern. Biochem J 356:387–394PubMedCrossRefGoogle Scholar
  49. Rehman S, Postma W, Tytgat T, Prins P, Qin L, Overmars H, Vossen J, Spiridon LN, Petrescu AJ, Goverse A, Bakker J, Smant G. (2009) A secreted SPRY domain-containing protein (SPRYSEC) from the plant-parasitic nematode Globodera rostochiensis interacts with a CC-NB-LRR protein from a susceptible tomato. Mol Plant-Mic Interact 22:330–340CrossRefGoogle Scholar
  50. Rice SL, Leadbeater BSC, Stone AR (1985) Changes in cell structure in roots of resistant potatoes parasitized by potato cyst-nematodes. I. Potatoes with resistance gene H1 derived from Solanum tuberosum ssp. andigena. Physiol Plant Pathol 27:219–234CrossRefGoogle Scholar
  51. Robertson L, Robertson WM, Sobczak M, Bakker J, Tetaud E, Arinagayayam MR, Ferguson MAJ, Fairlamb AH, Jones JT (2000) Cloning, expression and functional characterisation of a thioredoxin peroxidase from the potato cyst nematode Globodera rostochiensis. Mol Biochem Parasitol 111:41–49PubMedCrossRefGoogle Scholar
  52. Rooney HCE, van’t Klooster JW, van der Hoorn RAL, Joosten MHAJ, Jones JDG, de Wit PJGM (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1785–1786CrossRefGoogle Scholar
  53. Sacco MA, Koropacka K, Grenier E, Jaubert MJ, Blanchard A, Goverse A, Smant G, Moffett P (2009) The Cyst Nematode SPRYSEC Protein RBP-1 Elicits Gpa2- and RanGAP2-Dependent Plant Cell Death. PLoS Pathogens 5:e1000564CrossRefGoogle Scholar
  54. Semblat J-P, Rosso M-N, Hussey, RS Abad P, Castagnone-Sereno P (2001) Molecular cloning of a cDNA encoding an amphid secreted putative avirulence protein from the root knot nematode Meloidogyne incognita. Mol Plant-Mic Interact 14:72–79CrossRefGoogle Scholar
  55. Shibuya N, Minami E (2001) Oligosaccharide signalling for defence responses in plant. Physiol MolPlant Pathol 59:223–233CrossRefGoogle Scholar
  56. Song J, Win J, Tian M, Schornak S, Kaschani Fm Ilyas M, van der Hoorn R, Kamoun S (2009) Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defence protease Rcr3. Proc Nat Acad Sci U S A 106:1654–1659CrossRefGoogle Scholar
  57. Spallek T, Robatzek S, Gohre V (2009) How microbes utilize host ubiquitination. Cell Microbiol 11:1425–1434PubMedCrossRefGoogle Scholar
  58. Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groenendijk P, Reijans M, Fierens-Onstenk J, de Both M, Peleman J, Liharska T, Hontelez J, Zabeau M (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nature Biotechnol 16:1365–1369CrossRefGoogle Scholar
  59. Waetzig GH, Sobczak M, Grundler FMW (1999) Localization of hydrogen peroxide during the defence response of Arabidopsis thaliana against the plant parasitic nematode Heterodera glycines. Nematology 1:681–686CrossRefGoogle Scholar
  60. Whisson SC, Boevink PC, Moleleki L, Avrova A, 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 450:115–118PubMedCrossRefGoogle Scholar
  61. Wubben MJE, Jin J, Baum TJ (2008) Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid and elicits uncoupled SA independent pathogenesis related gene expression in roots. Mol Plant-Mic Interact 21:424–432CrossRefGoogle Scholar
  62. Wuyts N, Swennen R, De Waele D (2006) Effects of plant phenylpropanoid pathway products and selected terpenoids and alkaloids on the behaviour of the plant-parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne incognita. Nematology 8:89–101CrossRefGoogle Scholar
  63. Wuyts N, Lognay G, Verscheure M, Marlier M, De Waele D, Swennen R (2007) Potential physical and chemical barriers to infection by the burrowing nematode Radopholus similis in roots of susceptible and resistant banana (Musa spp). Plant Pathol 56:878–890CrossRefGoogle Scholar
  64. Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12:414–420PubMedCrossRefGoogle Scholar
  65. 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

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Laboratory of NematologyWageningen UniversityWageningenThe Netherlands
  2. 2.Plant Pathology Programme InvergowrieSCRIDundeeUK

Personalised recommendations