Plant-parasitic nematodes engage in prolonged and intimate relationships with their host plants, often involving complex alterations in host cell morphology and function. It is puzzling how nematodes can achieve this, seemingly without activating the innate immune system of their hosts. Secretions released by infective juvenile nematodes are thought to be crucial for host invasion, for nematode migration inside plants, and for feeding on host cells. In the past, much of the research focused on the manipulation of developmental pathways in host plants by plant-parasitic nematodes. However, recent findings demonstrate that plant-parasitic nematodes also deliver effectors into the apoplast and cytoplasm of host cells to suppress plant defense responses. In this review, we describe the current insights in the molecular and cellular mechanisms underlying the activation and suppression of host innate immunity by plant-parasitic nematodes along seven critical evolutionary and developmental transitions in plant parasitism.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Ali MA, Abbas A, Kreil DP, Bohlmann H. 1.  2013. Overexpression of the transcription factor RAP2.6 leads to enhanced callose deposition in syncytia and enhanced resistance against the beet cyst nematode Heterodera schachtii in Arabidopsis roots. BMC Plant Biol. 13:47 [Google Scholar]
  2. Alkharouf NW, Klink VP, Chouikha IB, Beard HS, MacDonald MH. 2.  et al. 2006. Timecourse microarray analyses reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 224:838–52 [Google Scholar]
  3. Arguel MJ, Jaouannet M, Magliano M, Abad P, Rosso MN. 3.  2012. siRNAs trigger efficient silencing of a parasitism gene in plant parasitic root-knot nematodes. Genes 3:391–408 [Google Scholar]
  4. Bakker J, Folkertsma RT, Rouppe van der Voort JNAM, de Boer JM, Gommers FJ. 4.  1993. Changing concepts and molecular approaches in the management of virulence genes in potato cyst nematodes. Annu. Rev. Phytopathol. 31:169–90 [Google Scholar]
  5. Bellafiore S, Shen Z, Rosso MN, Abad P, Shih P, Briggs SP. 5.  2008. Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathog. 4:e1000192 [Google Scholar]
  6. Bhattarai KK, Atamian HS, Kaloshian I, Eulgem T. 6.  2010. WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. Plant J. 63:229–40 [Google Scholar]
  7. Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I. 7.  2007. The Mi-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol. 144:312–23 [Google Scholar]
  8. Bhattarai KK, Xie QG, Mantelin S, Bishnoi U, Girke T. 8.  et al. 2008. Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Mol. Plant-Microbe Interact. 21:1205–14 [Google Scholar]
  9. Bird DM. 9.  1996. Manipulation of host gene expression by root-knot nematodes. J. Parasitol. 82:881–88 [Google Scholar]
  10. Bleve-Zacheo T, Bongiovanni M, Melillo MT, Castagnone-Sereno P. 10.  1998. The pepper resistance genes Me1 and Me3 induce differential penetration rates and temporal sequences of root cell ultrastructural changes upon nematode infection. Plant Sci. 133:79–90 [Google Scholar]
  11. Boller T, Felix G. 11.  2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379–407 [Google Scholar]
  12. Boudsocq M, Sheen J. 12.  2013. CDPKs in immune and stress signaling. Trends Plant Sci. 18:30–40 [Google Scholar]
  13. Bouwmeester K, Govers F. 13.  2009. Arabidopsis L-type lectin receptor kinases: phylogeny, classification, and expression profiles. J. Exp. Bot. 60:4383–96 [Google Scholar]
  14. Cai D, Kleine M, Kifle S, Harloff HJ, Sandal NN. 14.  et al. 1997. Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832–34 [Google Scholar]
  15. Cantacessi C, Campbell BE, Visser A, Geldhof P, Nolan MJ. 15.  et al. 2009. A portrait of the “SCP/TAPS” proteins of eukaryotes: developing a framework for fundamental research and biotechnological outcomes. Biotechnol. Adv. 27:376–88 [Google Scholar]
  16. Carpentier J, Esquibet M, Fouville D, Manzanares-Dauleux MJ, Kerlan MC, Grenier E. 16.  2012. The evolution of the Gp-Rbp-1 gene in Globodera pallida includes multiple selective replacements. Mol. Plant Pathol. 13:546–55 [Google Scholar]
  17. Casteel CL, Walling LL, Paine TD. 17.  2006. Behavior and biology of the tomato psyllid, Bactericera cockerelli, in response to the Mi-1.2 gene. Entomol. Exp. Appl. 121:67–72 [Google Scholar]
  18. Castelli L, Bryan G, Blok VC, Ramsay G, Phillips MS. 18.  2005. Investigation of resistance specificity amongst fifteen wild Solanum species to a range of Globodera pallida and G. rostochiensis populations. Nematology 7:689–99 [Google Scholar]
  19. Chen S, Chronis D, Wang X. 19.  2013. The novel GrCEP12 peptide from the plant-parasitic nematode Globodera rostochiensis suppresses flg22-mediated PTI. Plant Signal. Behav. 8:e25359 [Google Scholar]
  20. Chronis D, Chen SY, Lu SW, Hewezi T, Carpenter SCD. 20.  et al. 2013. A ubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism. Plant J. 74:185–96 [Google Scholar]
  21. Claverie M, Dirlewanger E, Bosselut N, van Ghelder C, Voisin R. 21.  et al. 2011. The Ma gene for complete-spectrum resistance to Meloidogyne species in Prunus is a TNL with a huge repeated C-terminal post-LRR region. Plant Physiol. 156:779–92 [Google Scholar]
  22. Cohn E, Kaplan DT, Esser RP. 22.  1984. Observations on the mode of parasitism and histopathology of Meloidodera floridensis and Verutus volvingentis (Heteroderidae). J. Nematol. 16:256–64 [Google Scholar]
  23. Collier SM, Moffett P. 23.  2009. NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci. 14:521–29 [Google Scholar]
  24. Cook DE, Geon Lee T, Guo X, Melito S, Wang K. 24.  et al. 2012. Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–9 [Google Scholar]
  25. Cookson E, Blaxter ML, Selkirk ME. 25.  1992. Identification of the major soluble cuticular glycoprotein (gp29) as a secretory homolog of glutathione peroxidase. Proc. Natl. Acad. Sci. USA 89:5837–41 [Google Scholar]
  26. Das S, DeMason DA, Ehlers JD, Close TJ, Roberts PA. 26.  2008. Histological characterization of root-knot nematode resistance in cowpea and its relation to reactive oxygen species modulation. J. Exp. Bot. 59:1305–13 [Google Scholar]
  27. Davies KG, Curtis RHC. 27.  2011. Cuticle surface coat of plant-parasitic nematodes. Annu. Rev. Phytopathol. 49:135–56 [Google Scholar]
  28. De Boer JM, Overmars HA, Bakker J, Gommers FJ. 28.  1992. Analysis of two-dimensional protein patterns from developmental stages of the potato cyst-nematode, Globodera rostochiensis. Parasitology 105:461–74 [Google Scholar]
  29. De Ilarduya OM, Moore AE, Kaloshian I. 29.  2001. The tomato Rme1 locus is required for Mi-1-mediated resistance to root-knot nematodes and the potato aphid. Plant J. 27:417–25 [Google Scholar]
  30. de la Torre F, Gutiérrez-Beltrán E, Pareja-Jaime Y, Chakravarthy S, Martin GB, del Pozo O. 30.  2013. The tomato calcium sensor Cbl10 and its interacting protein kinase cipk6 define a signaling pathway in plant immunity. Plant Cell 25:2748–64 [Google Scholar]
  31. Dropkin VH. 31.  1969. The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology 59:1632–37 [Google Scholar]
  32. Dubreuil G, Deleury E, Magliano M, Jaouannet M, Abad P, Rosso MN. 32.  2011. Peroxiredoxins from the plant parasitic root-knot nematode, Meloidogyne incognita, are required for successful development within the host. Int. J. Parasitol. 41:385–96 [Google Scholar]
  33. Dubreuil G, Magliano M, Deleury E, Abad P, Rosso MN. 33.  2007. Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism. New Phytol. 176:426–36 [Google Scholar]
  34. Dudler R. 34.  2013. Manipulation of host proteasomes as a virulence mechanism of plant pathogens. Annu. Rev. Phytopathol. 51:521–42 [Google Scholar]
  35. Ellinger D, Naumann M, Falter C, Zwikowics C, Jamrow T. 35.  et al. 2013. Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiol. 161:1433–44 [Google Scholar]
  36. Endo BY, Wyss U. 36.  1992. Ultrastructure of cuticular exudations in parasitic juvenile Heterodera schachtii, as related to cuticle structure. Protoplasma 166:67–77 [Google Scholar]
  37. Ernst K, Kumar A, Kriseleit D, Kloos DU, Phillips MS, Ganal MW. 37.  2002. The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J. 31:127–36 [Google Scholar]
  38. Eulgem T, Somssich IE. 38.  2007. Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10:366–71 [Google Scholar]
  39. Finkers-Tomczak A, Bakker E, de Boer J, van der Vossen E, Achenbach U. 39.  et al. 2011. Comparative sequence analysis of the potato cyst nematode resistance locus H1 reveals a major lack of co-linearity between three haplotypes in potato (Solanum tuberosum ssp.). Theor. Appl. Genet. 122:595–608 [Google Scholar]
  40. Forrest JMS, Robertson WM, Milne EW. 40.  1989. Changes in the structure of amphidial exudate and the nature of lectin labelling on freshly hatched, invaded and emigrant second stage juveniles of Globodera rostochiensis. Nematologica 34:422–31 [Google Scholar]
  41. Fudali SL, Wang CL, Williamson VM. 41.  2013. Ethylene signaling pathway modulates attractiveness of host roots to the root-knot nematode Meloidogyne hapla. Mol. Plant-Microbe Interact. 26:75–86 [Google Scholar]
  42. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS. 42.  2003. The parasitome of the phytonematode Heterodera glycines. Mol. Plant-Microbe Interact. 16:720–26 [Google Scholar]
  43. Gheysen G, Mitchum MG. 43.  2011. How nematodes manipulate plant development pathways for infection. Curr. Opin. Plant Biol. 14:415–21 [Google Scholar]
  44. Gish LA, Clark SE. 44.  2011. The RLK/Pelle family of kinases. Plant J. 66:117–27 [Google Scholar]
  45. Goto DB, Miyazawa H, Mar JC, Sato M. 45.  2013. Not to be suppressed? Rethinking the host response at a root-parasite interface. Plant Sci. 213:9–17 [Google Scholar]
  46. Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder J. 46.  2000. Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Mol. Plant-Microbe Interact. 13:1121–29 [Google Scholar]
  47. Grundler FMW, Betka M, Wyss U. 47.  1991. Influence of changes in the nurse cell system (syncytium) on sex determination and development of the cyst nematode Heterodera schachtii: total amounts of proteins and amino acids. Phytopathology 81:70–74 [Google Scholar]
  48. Grundler FMW, Sobczak M, Lange S. 48.  1997. Defence responses of Arabidopsis thaliana during invasion and feeding site induction by the plant-parasitic nematode Heterodera glycines. Physiol. Mol. Plant Pathol. 50:419–29 [Google Scholar]
  49. Haegeman A, Jacob J, Vanholme B, Kyndt T, Mitreva M, Gheysen G. 49.  2009. Expressed sequence tags of the peanut pod nematode Ditylenchus africanus: the first transcriptome analysis of an anguinid nematode. Mol. Biochem. Parasitol. 167:32–40 [Google Scholar]
  50. Haegeman A, Jones JT, Danchin EGJ. 50.  2011. Horizontal gene transfer in nematodes: a catalyst for plant parasitism?. Mol. Plant-Microbe Interact. 24:879–87 [Google Scholar]
  51. Haegeman A, Joseph S, Gheysen G. 51.  2011. Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Mol. Biochem. Parasitol. 178:7–14 [Google Scholar]
  52. Hamamouch N, Li CY, Hewezi T, Baum TJ, Mitchum MG. 52.  et al. 2012. The interaction of the novel 30C02 cyst nematode effector protein with a plant β-1,3-endoglucanase may suppress host defence to promote parasitism. J. Exp. Bot. 63:3683–95 [Google Scholar]
  53. Hansen E, Harper G, McPherson MJ, Atkinson HJ. 53.  1996. Differential expression patterns of the wound-inducible transgene wun1-uidA in potato roots following infection with either cyst or root knot nematodes. Physiol. Mol. Plant Pathol. 48:161–70 [Google Scholar]
  54. Hayes JD, Flanagan JU, Jowsey IR. 54.  2005. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45:51–88 [Google Scholar]
  55. Heil M. 55.  2009. Damaged-self recognition in plant herbivore defence. Trends Plant Sci. 14:356–63 [Google Scholar]
  56. Henkle-Dührsen K, Kampkotter A. 56.  2001. Antioxidant enzyme families in parasitic nematodes. Mol. Biochem. Parasitol. 114:129–42 [Google Scholar]
  57. Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG. 57.  et al. 2010. Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol. 152:968–84 [Google Scholar]
  58. Holscher D, Dhakshinamoorthy S, Alexandrov T, Becker M, Bretschneider T. 58.  et al. 2013. Phenalenone-type phytoalexins mediate resistance of banana plants (Musa spp.) to the burrowing nematode Radopholus similis. Proc. Natl. Acad. Sci. USA 111:105–110 [Google Scholar]
  59. Hussey RS. 59.  1989. Disease-inducing secretions of plant-parasitic nematodes. Annu. Rev. Phytopathol. 27:123–41 [Google Scholar]
  60. Hussey RS, Mims CW, Westcott SWI. 60.  1992. Ultrastructure of root cortical cells parasitized by the ring nematode Criconemella xenoplax. Protoplasma 167:55–65 [Google Scholar]
  61. Iberkleid I, Vieira P, de Almeida Engler J, Firester K, Spiegel Y, Horowitz SB. 61.  2013. Fatty acid– and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes. PLoS ONE 8:e64586 [Google Scholar]
  62. Ithal N, Recknor J, Nettleton D, Hearne L, Maier T. 62.  et al. 2007. Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol. Plant-Microbe Interact. 20:293–305 [Google Scholar]
  63. Jaouannet M, Magliano M, Arguel MJ, Gourgues M, Evangelisti E. 63.  et al. 2013. The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Mol. Plant-Microbe Interact. 26:97–105 [Google Scholar]
  64. Jasmer DP, Goverse A, Smant G. 64.  2003. Parasitic nematode interactions with mammals and plants. Annu. Rev. Phytopathol. 41:245–70 [Google Scholar]
  65. Jaubert S, Ledger TN, Laffaire JB, Piotte C, Abad P, Rosso MN. 65.  2002. Direct identification of stylet secreted proteins from root-knot nematodes by a proteomic approach. Mol. Biochem. Parasitol. 121:205–11 [Google Scholar]
  66. Jaubert S, Milac AL, Petrescu AJ, de Almeida-Engler J, Abad P, Rosso MN. 66.  2005. In planta secretion of a calreticulin by migratory and sedentary stages of root-knot nematode. Mol. Plant-Microbe Interact. 18:1277–84 [Google Scholar]
  67. Jones JDG, Dangl JL. 67.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  68. Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J. 68.  et al. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Mol. Plant Pathol. 14:946–61 [Google Scholar]
  69. Jones JT, Kumar A, Pylypenko LA, Thirugnanasambandam A, Castelli L. 69.  et al. 2009. Identification and functional characterization of effectors in expressed sequence tags from various life cycle stages of the potato cyst nematode Globodera pallida. Mol. Plant Pathol. 10:815–28 [Google Scholar]
  70. Jones JT, Reavy B, Smant G, Prior AE. 70.  2004. Glutathione peroxidases of the potato cyst nematode Globodera rostochiensis. Gene 324:47–54 [Google Scholar]
  71. Jones MGK, Northcote DH. 71.  1972. Nematode-induced syncytium: a multinucleate transfer cell. J. Cell Sci. 10:789–809 [Google Scholar]
  72. Kandoth PK, Ithal N, Recknor J, Maier T, Nettleton D. 72.  et al. 2011. The soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates the expression of a large number of stress- and defense-related genes in degenerating feeding cells. Plant Physiol. 155:1960–75 [Google Scholar]
  73. Kandoth PK, Mitchum MG. 72a.  2013. War of the worms: how plants flight underground attacks. Curr. Opin. Plant Biol. 16:457–63 [Google Scholar]
  74. Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S. 73.  2004. Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol. 45:712–22 [Google Scholar]
  75. Khallouk S, Voisin R, Van Ghelder C, Engler G, Amiri S, Esmenjaud D. 74.  2011. Histological mechanisms of the resistance conferred by the Ma gene against Meloidogyne incognita in Prunus spp. Phytopathology 101:945–51 [Google Scholar]
  76. Koropacka K. 75.  2010. Molecular contest between potato and potato cyst nematode Globodera pallida: modulation of Gpa2-mediated resistance PhD Thesis, Wageningen Univ., Wageningen 132 [Google Scholar]
  77. Kouassi AB, Kerlan MC, Sobczak M, Dantec JP, Rouaux C. 76.  et al. 2004. Resistance to the root-knot nematode Meloidogyne fallax in Solanum sparsipilum: analysis of the mechanisms. Nematology 6:389–400 [Google Scholar]
  78. Kruger J, Thomas CM, Golstein C, Dixon MS, Smoker M. 77.  et al. 2002. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296:744–47 [Google Scholar]
  79. Kyndt T, Vieira P, Gheysen G, de Almeida-Engler J. 78.  2013. Nematode feeding sites: unique organs in plant roots. Planta 238:807–18 [Google Scholar]
  80. Lambert KN, Ferrie BJ, Nombela G, Brenner ED, Williamson VM. 79.  1999. Identification of genes whose transcripts accumulate rapidly in tomato after root-knot nematode infection. Physiol. Mol. Plant Pathol. 55:341–48 [Google Scholar]
  81. Lecourieux D, Ranjeva R, Pugin A. 80.  2006. Calcium in plant defence-signalling pathways. New Phytol. 171:249–69 [Google Scholar]
  82. Li Q, Xie QG, Smith-Becker J, Navarre DA, Kaloshian I. 81.  2006. Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol. Plant-Microbe Interact. 19:655–64 [Google Scholar]
  83. Li X, Zhuo K, Luo M, Sun L, Liao J. 82.  2011. Molecular cloning and characterization of a calreticulin cDNA from the pinewood nematode Bursaphelenchus xylophilus. Exp. Parasitol. 128:121–26 [Google Scholar]
  84. Li Z, Liu X, Chu Y, Wang Y, Zhang Q, Zhou X. 83.  2011. Cloning and characterization of a 2-Cys peroxiredoxin in the pine wood nematode, Bursaphelenchus xylophilus, a putative genetic factor facilitating the infestation. Int. J. Biol. Sci. 7:823–36 [Google Scholar]
  85. Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R. 84.  et al. 2012. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492:256–60 [Google Scholar]
  86. Lozano-Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Finkers-Tomczak A. 85.  et al. 2012. Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. Proc. Natl. Acad. Sci. USA 109:10119–24 [Google Scholar]
  87. Lukasik-Shreepaathy E, Slootweg E, Richter H, Goverse A, Cornelissen BJC, Takken FLW. 86.  2012. Dual regulatory roles of the extended N terminus for activation of the tomato Mi-1.2 resistance protein. Mol. Plant-Microbe Interact. 25:1045–57 [Google Scholar]
  88. Mahalingam R, Skorupska HT. 87.  1996. Cytological expression of early response to infection by Heterodera glycines Ichinohe in resistant PI 437654 soybean. Genome 39:986–98 [Google Scholar]
  89. Mantelin S, Peng HC, Li B, Atamian HS, Takken FLW, Kaloshian I. 88.  2011. The receptor-like kinase SlSERK1 is required for Mi-1-mediated resistance to potato aphids in tomato. Plant J. 67:459–71 [Google Scholar]
  90. Martinez de Ilarduya O, Nombela G, Hwang CF, Williamson VM, Muñiz M, Kaloshian I. 89.  2004. Rme1 is necessary for Mi-1-mediated resistance and acts early in the resistance pathway. Mol. Plant-Microbe Interact. 17:55–61 [Google Scholar]
  91. Matsye PD, Lawrence GW, Youssef RM, Kim KH, Lawrence KS. 90.  et al. 2012. The expression of a naturally occurring, truncated allele of an α-SNAP gene suppresses plant parasitic nematode infection. Plant Mol. Biol. 80:131–55 [Google Scholar]
  92. Melillo MT, Leonetti P, Bongiovanni M, Castagnone-Sereno P, Bleve-Zacheo T. 91.  2006. Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato-root-knot nematode interactions. New Phytol. 170:501–12 [Google Scholar]
  93. Melillo MT, Leonetti P, Leone A, Veronico P, Bleve-Zacheo T. 92.  2011. ROS and NO production in compatible and incompatible tomato–Meloidogyne incognita interactions. Eur. J. Plant Pathol. 130:489–502 [Google Scholar]
  94. Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM. 93.  1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–19 [Google Scholar]
  95. Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA. 94.  et al. 2013. Nematode effector proteins: an emerging paradigm of parasitism. New Phytol. 199:879–94 [Google Scholar]
  96. Monaghan J, Zipfel C. 95.  2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:349–57 [Google Scholar]
  97. Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA. 96.  2008. Plant polyamine catabolism: the state of the art. Plant Signal. Behav. 3:1061–66 [Google Scholar]
  98. Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J. 97.  et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596–601 [Google Scholar]
  99. Mylonas C, Kouretas D. 98.  1999. Lipid peroxidation and tissue damage. In Vivo 13:295–309 [Google Scholar]
  100. Neher DA. 99.  2010. Ecology of plant and free-living nematodes in natural and agricultural soil. Annu. Rev. Phytopathol. 48:371–94 [Google Scholar]
  101. Nishimura MT, Dangl JL. 100.  2010. Arabidopsis and the plant immune system. Plant J. 61:1053–66 [Google Scholar]
  102. Nombela G, Williamson VM, Muñiz M. 101.  2003. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol. Plant-Microbe Interact. 16:645–49 [Google Scholar]
  103. Offler CE, McCurdy DW, Patrick JW, Talbot MJ. 102.  2003. Transfer cells: cells specialized for a special purpose. Annu. Rev. Plant Biol. 54:431–54 [Google Scholar]
  104. Paal J, Henselewski H, Muth J, Meksem K, Menéndez CM. 103.  et al. 2004. Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J. 38:285–97 [Google Scholar]
  105. Patel N, Hamamouch N, Li C, Hewezi T, Hussey RS. 104.  et al. 2010. A nematode effector protein similar to annexins in host plants. J. Exp. Bot. 61:235–48 [Google Scholar]
  106. Paulson RE, Webster JM. 105.  1972. Ultrastructure of the hypersensitive reaction in roots of tomato, Lyco-persicon esculentum L., to infection by the root-knot nematode, Meloidogyne incognita. Physiol. Plant Pathol. 2:227–34 [Google Scholar]
  107. Peng H, Gao BL, Kong LA, Yu Q, Huang WK. 106.  et al. 2013. Exploring the host parasitism of the migratory plant-parasitic nematode Ditylenchus destructor by expressed sequence tags analysis. PLoS ONE 8:e69579 [Google Scholar]
  108. Perry RN. 107.  1989. Dormancy and hatching of nematode eggs. Parasitol. Today 5:377–83 [Google Scholar]
  109. Postma WJ, Slootweg EJ, Rehman S, Finkers-Tomczak A, Tytgat TO. 108.  et al. 2012. The effector SPRYSEC-19 of Globodera rostochiensis suppresses CC-NB-LRR-mediated disease resistance in plants. Plant Physiol. 160:944–54 [Google Scholar]
  110. Prior A, Jones JT, Blok VC, Beauchamp J, McDermott L. 109.  et al. 2001. A surface-associated retinol- and fatty acid–binding protein (Gp-FAR-1) from the potato cyst nematode Globodera pallida: lipid binding activities, structural analysis and expression pattern. Biochem. J. 356:387–94 [Google Scholar]
  111. Rairdan GJ, Moffett P. 110.  2006. Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell 18:2082–93 [Google Scholar]
  112. Ramírez V, López A, Mauch-Mani B, Gil MJ, Vera P. 111.  2013. An extracellular subtilase switch for immune priming in Arabidopsis. PLoS Pathog. 9:e1603445 [Google Scholar]
  113. Rehman S, Butterbach P, Popeijus H, Overmars H, Davis EL. 112.  et al. 2009. Identification and characterization of the most abundant cellulases in stylet secretions from Globodera rostochiensis. Phytopathology 99:194–202 [Google Scholar]
  114. Rehman S, Postma W, Tytgat T, Prins P, Qin L. 113.  et al. 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-Microbe Interact. 22:330–40 [Google Scholar]
  115. Reinbothe C, Springer A, Samol I, Reinbothe S. 114.  2009. Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence. FEBS J. 276:4666–81 [Google Scholar]
  116. Rice SL, Leadbeater BSC, Stone AR. 115.  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. Mol. Plant Pathol. 27:219–34 [Google Scholar]
  117. Robertson L, Robertson WM, Sobczak M, Helder J, Tetaud E. 116.  et al. 2000. Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis. Mol. Biochem. Parasitol. 111:41–49 [Google Scholar]
  118. Rooney HC, Van't Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, de Wit PJ. 117.  2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783–86 [Google Scholar]
  119. Sacco MA, Koropacka K, Grenier E, Jaubert MJ, Blanchard A. 118.  et al. 2009. The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathog. 5:e1000564 [Google Scholar]
  120. Schulz P, Herde M, Romeis T. 119.  2013. Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol. 163:523–30 [Google Scholar]
  121. Schwessinger B, Zipfel C. 120.  2008. News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 11:389–95 [Google Scholar]
  122. Sheridan JP, Miller AJ, Perry RN. 121.  2004. Early responses of resistant and susceptible potato roots during invasion by the potato cyst nematode Globodera rostochiensis. J. Exp. Bot. 55:751–60 [Google Scholar]
  123. Sijmons PC, Atkinson HJ, Wyss U. 122.  1994. Parasitic strategies of root nematodes and associated host cell responses. Annu. Rev. Phytopathol. 32:235–59 [Google Scholar]
  124. Slootweg EJ, Spiridon LN, Roosien J, Butterbach P, Pomp R. 123.  et al. 2013. Structural determinants at the interface of the ARC2 and leucine-rich repeat domains control the activation of the plant immune receptors Rx1 and Gpa2. Plant Physiol. 162:1510–28 [Google Scholar]
  125. Sobczak M, Avrova A, Jupowicz J, Phillips MS, Ernst K, Kumar A. 124.  2005. Characterization of susceptibility and resistance responses to potato cyst nematode (Globodera spp.) infection of tomato lines in the absence and presence of the broad-spectrum nematode resistance Hero gene. Mol. Plant-Microbe Interact. 18:158–68 [Google Scholar]
  126. Takken FLW, Goverse A. 125.  2012. How to build a pathogen detector: structural basis of NB-LRR function. Curr. Opin. Plant Biol. 15:375–84 [Google Scholar]
  127. Tameling WIL, Elzinga SDJ, Darmin PS, Vossen JH, Takken FLW. 126.  et al. 2002. The tomato R gene products i-2 and Mi-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14:2929–39 [Google Scholar]
  128. Tang L, Smith VP, Gounaris K, Selkirk ME. 127.  1996. Brugia pahangi: the cuticular glutathione peroxidase (gp29) protects heterologous membranes from lipid peroxidation. Exp. Parasitol. 82:329–32 [Google Scholar]
  129. Thomma BPHJ, Nürnberger T, Joosten MHAJ. 128.  2011. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15 [Google Scholar]
  130. Torres MA, Jones JDG, Dangl JL. 129.  2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141:373–78 [Google Scholar]
  131. Trudgill DL. 130.  1967. The effect of environment on sex determination in Heterodera rostochiensis. Nematologica 13:263–72 [Google Scholar]
  132. Turk B, Turk D, Turk V. 131.  2012. Protease signalling: the cutting edge. EMBO J. 31:1630–43 [Google Scholar]
  133. Tytgat T, Vanholme B, De Meutter J, Claeys M, Couvreur M. 132.  et al. 2004. A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant parasitic cyst nematodes. Mol. Plant-Microbe Interact. 17:846–52 [Google Scholar]
  134. van der Hoorn RA, Jones JD. 133.  2004. The plant proteolytic machinery and its role in defence. Curr. Opin. Plant Biol. 7:400–7 [Google Scholar]
  135. van der Hoorn RA, Kamoun S. 134.  2008. From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–17 [Google Scholar]
  136. van der Vossen EAG, van der Voort JNAM, Kanyuka K, Bendahmane A, Sandbrink H. 135.  et al. 2000. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J. 23:567–76 [Google Scholar]
  137. van Esse HP, Van't Klooster JW, Bolton MD, Yadeta KA, van Baarlen P. 136.  et al. 2008. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20:1948–63 [Google Scholar]
  138. Van Loon LC, Rep M, Pieterse CMJ. 137.  2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135–62 [Google Scholar]
  139. van Megen H, van den Elsen S, Holterman M, Karssen G, Mooyman P. 138.  et al. 2009. A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927–50 [Google Scholar]
  140. Vieira P, Escudero C, Rodiuc N, Boruc J, Russinova E. 139.  et al. 2013. Ectopic expression of Kip-related proteins restrains root-knot nematode-feeding site expansion. New Phytol. 199:505–19 [Google Scholar]
  141. Vieira P, Kyndt T, Gheysen G, de Almeida Engler J. 140.  2013. An insight into critical endocycle genes for plant-parasitic nematode feeding sites establishment. Plant Signal. Behav. 8:e242231 [Google Scholar]
  142. Vierstra RD. 141.  2009. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10:385–97 [Google Scholar]
  143. Vos C, Van den Broucke D, Lombi FM, De Waele D, Elsen A. 142.  2012. Mycorrhiza-induced resistance in banana acts on nematode host location and penetration. Soil Biol. Biochem. 47:60–66 [Google Scholar]
  144. Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L. 143.  et al. 1998. The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat. Biotechnol. 16:1365 [Google Scholar]
  145. Waetzig GH, Sobczak M, Grundler FMW. 144.  1999. Localization of hydrogen peroxide during the defence response of Arabidopsis thaliana against the plant-parasitic nematode Heterodera glycines. Nematology 1:681–86 [Google Scholar]
  146. Williamson VM, Hussey RS. 145.  1996. Nematode pathogenesis and resistance in plants. Plant Cell 8:1735–45 [Google Scholar]
  147. Williamson VM, Kumar A. 146.  2006. Nematode resistance in plants: the battle underground. Trends Genet. 22:396–403 [Google Scholar]
  148. Woo JS, Imm JH, Min CK, Kim KJ, Cha SS, Oh BH. 147.  2006. Structural and functional insights into the B30.2/SPRY domain. EMBO J. 25:1353–63 [Google Scholar]
  149. Wubben MJE II, Su H, Rodermel SR, Baum TJ. 148.  2001. Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 14:1206–12 [Google Scholar]
  150. Wyss U, Grundler FMW. 149.  1992. Feeding behaviour of sedentary plant parasitic nematodes. Neth. J. Plant Pathol. 98:Suppl. 2165–73 [Google Scholar]
  151. Zunke U. 150.  1990. Observations on the invasion and endoparasitic behaviour of the root lesion nematode Pratylenchus penetrans. J. Nematol. 22:309–20 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error