The activation and suppression of plant innate immunity by parasitic nematodes

Annual Review of Phytopathology

Volumn 52, Issue , 2014, Pages 243-265

  Goverse, Aska ^a   Smant, Geert ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Defense; Effector; Excretory secretory proteins; Host target; Resistance; Virulence

Indexed keywords

ADAPTATION; ANIMAL; HOST PARASITE INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; NEMATODE; PARASITOLOGY; PHYSIOLOGY; PLANT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; NEMATODA; PLANTS;

EID: 84905513422     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-102313-050118     Document Type: Article

References (151)

1. Ali MA, Abbas A, Kreil DP, Bohlmann H. 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
2. Alkharouf NW, Klink VP, Chouikha IB, Beard HS, MacDonald MH, 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
3. Arguel MJ, Jaouannet M, Magliano M, Abad P, Rosso MN. 2012. siRNAs trigger efficient silencing of a parasitism gene in plant parasitic root-knot nematodes. Genes 3:391-408
4. Bakker J, Folkertsma RT, Rouppe van der Voort JNAM, de Boer JM, Gommers FJ. 1993. Changing concepts and molecular approaches in the management of virulence genes in potato cyst nematodes. Annu. Rev. Phytopathol. 31:169-90
5. Bellafiore S, Shen Z, Rosso MN, Abad P, Shih P, Briggs SP. 2008. Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathog. 4:e1000192
6. Bhattarai KK, Atamian HS, Kaloshian I, Eulgem T. 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
7. Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I. 2007. The Mi-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol. 144:312-23
8. Bhattarai KK, Xie QG, Mantelin S, Bishnoi U, Girke T, et al. 2008. Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Mol. Plant-Microbe Interact. 21:1205-14
9. Bird DM. 1996. Manipulation of host gene expression by root-knot nematodes. J. Parasitol. 82:881-88
10. Bleve-Zacheo T, Bongiovanni M, Melillo MT, Castagnone-Sereno P. 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
11. 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. 60:379-407
12. Boudsocq M, Sheen J. 2013. CDPKs in immune and stress signaling. Trends Plant Sci. 18:30-40
13. Bouwmeester K, Govers F. 2009. Arabidopsis L-type lectin receptor kinases: phylogeny, classification, and expression profiles. J. Exp. Bot. 60:4383-96
14. Cai D, Kleine M, Kifle S, Harloff HJ, Sandal NN, et al. 1997. Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832-34
15. Cantacessi C, Campbell BE, Visser A, Geldhof P, Nolan MJ, 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
16. Carpentier J, Esquibet M, Fouville D, Manzanares-Dauleux MJ, Kerlan MC, Grenier E. 2012. The evolution of the Gp-Rbp-1 gene in Globodera pallida includes multiple selective replacements. Mol. Plant Pathol. 13:546-55
17. Casteel CL, Walling LL, Paine TD. 2006. Behavior and biology of the tomato psyllid, Bactericera cockerelli, in response to the Mi-1.2 gene. Entomol. Exp. Appl. 121:67-72
18. Castelli L, Bryan G, Blok VC, Ramsay G, Phillips MS. 2005. Investigation of resistance specificity amongst fifteen wild Solanum species to a range of Globodera pallida and G. rostochiensis populations. Nematology 7:689-99
19. Chen S, Chronis D, Wang X. 2013. The novel GrCEP12 peptide from the plant-parasitic nematode Globodera rostochiensis suppresses flg22-mediated PTI. Plant Signal. Behav. 8:e25359
20. Chronis D, Chen SY, Lu SW, Hewezi T, Carpenter SCD, 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
21. Claverie M, Dirlewanger E, Bosselut N, van Ghelder C, Voisin R, et al. 2011. The Ma gene for completespectrum resistance to Meloidogyne species in Prunus is aTNLwith a huge repeated C-terminal post-LRR region. Plant Physiol. 156:779-92
22. Cohn E, Kaplan DT, Esser RP. 1984. Observations on the mode of parasitism and histopathology of Meloidodera floridensis and Verutus volvingentis (Heteroderidae). J. Nematol. 16:256-64
23. Collier SM, Moffett P. 2009. NB-LRRs work a "bait and switch" on pathogens. Trends Plant Sci. 14:521-29
24. Cook DE, Geon Lee T, Guo X, Melito S, Wang K, et al. 2012. Copy number variation ofmultiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206-9
25. Cookson E, Blaxter ML, Selkirk ME. 1992. Identification of the major soluble cuticular glycoprotein (gp29) as a secretory homolog of glutathione peroxidase. Proc. Natl. Acad. Sci. USA 89:5837-41
26. Das S, DeMason DA, Ehlers JD, Close TJ, Roberts PA. 2008. Histological characterization of rootknot nematode resistance in cowpea and its relation to reactive oxygen species modulation. J. Exp. Bot. 59:1305-13
27. Davies KG, Curtis RHC. 2011. Cuticle surface coat of plant-parasitic nematodes. Annu. Rev. Phytopathol. 49:135-56
28. De Boer JM, Overmars HA, Bakker J, Gommers FJ. 1992. Analysis of two-dimensional protein patterns from developmental stages of the potato cyst-nematode, Globodera rostochiensis. Parasitology 105:461-74
29. De Ilarduya OM, Moore AE, Kaloshian I. 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
30. de la Torre F, Gutierrez-Beltran E, Pareja-Jaime Y, Chakravarthy S, Martin GB, del Pozo O. 2013. The tomato calcium sensor Cbl10 and its interacting protein kinase cipk6 define a signaling pathway in plant immunity. Plant Cell 25:2748-64
31. Dropkin VH. 1969. The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology 59:1632-37
32. Dubreuil G, Deleury E, Magliano M, Jaouannet M, Abad P, Rosso MN. 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
33. 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. 176:426-36
34. Dudler R. 2013. Manipulation of host proteasomes as a virulence mechanism of plant pathogens. Annu. Rev. Phytopathol. 51:521-42
35. Ellinger D, Naumann M, Falter C, Zwikowics C, Jamrow T, et al. 2013. Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiol. 161:1433-44
36. Endo BY, Wyss U. 1992. Ultrastructure of cuticular exudations in parasitic juvenile Heterodera schachtii, as related to cuticle structure. Protoplasma 166:67-77
37. Ernst K, Kumar A, Kriseleit D, Kloos DU, Phillips MS, Ganal MW. 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
38. Eulgem T, Somssich IE. 2007. Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10:366-71
39. Finkers-Tomczak A, Bakker E, de Boer J, van der Vossen E, Achenbach U, 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
40. Forrest JMS, Robertson WM, Milne EW. 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
41. Fudali SL, Wang CL, Williamson VM. 2013. Ethylene signaling pathway modulates attractiveness of host roots to the root-knot nematode Meloidogyne hapla. Mol. Plant-Microbe Interact. 26:75-86
42. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS. 2003. The parasitome of the phytonematode Heterodera glycines. Mol. Plant-Microbe Interact. 16:720-26
43. Gheysen G, Mitchum MG. 2011. How nematodesmanipulate plant development pathways for infection. Curr. Opin. Plant Biol. 14:415-21
44. Gish LA, Clark SE. 2011. The RLK/Pelle family of kinases. Plant J. 66:117-27
45. Goto DB, Miyazawa H, Mar JC, Sato M. 2013. Not to be suppressed? Rethinking the host response at a root-parasite interface. Plant Sci. 213:9-17
46. Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder J. 2000. Both induction and morphogenesis of cyst nematode feeding cells aremediated by auxin. Mol. Plant-Microbe Interact. 13:1121-29
47. Grundler FMW, Betka M, Wyss U. 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
48. 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. 50:419-29
49. Haegeman A, Jacob J, Vanholme B, Kyndt T, Mitreva M, Gheysen G. 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
50. Haegeman A, Jones JT, Danchin EGJ. 2011. Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Mol. Plant-Microbe Interact. 24:879-87
51. Haegeman A, Joseph S, Gheysen G. 2011. Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Mol. Biochem. Parasitol. 178:7-14
52. Hamamouch N, Li CY, Hewezi T, Baum TJ, Mitchum MG, et al. 2012. The interaction of the novel 30C02 cyst nematode effector protein with a plant-1, 3-endoglucanase may suppress host defence to promote parasitism. J. Exp. Bot. 63:3683-95
53. Hansen E, Harper G, McPherson MJ, Atkinson HJ. 1996. Differential expression patterns of the woundinducible transgene wun1-uidA in potato roots following infection with either cyst or root knot nematodes. Physiol. Mol. Plant Pathol. 48:161-70
54. Hayes JD, Flanagan JU, Jowsey IR. 2005. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45:51-88
55. Heil M. 2009. Damaged-self recognition in plant herbivore defence. Trends Plant Sci. 14:356-63
56. Henkle-D uhrsen K, Kampkotter A. 2001. Antioxidant enzyme families in parasitic nematodes. Mol. Biochem. Parasitol. 114:129-42
57. Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG, et al. 2010. Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol. 152:968-84
58. Holscher D, Dhakshinamoorthy S, Alexandrov T, Becker M, Bretschneider T, et al. 2013. Phenalenonetype phytoalexinsmediate resistance of banana plants (Musa spp.) to the burrowing nematode Radopholus similis. Proc. Natl. Acad. Sci. USA 111:105-110
59. Hussey RS. 1989. Disease-inducing secretions of plant-parasitic nematodes. Annu. Rev. Phytopathol. 27:123-41
60. Hussey RS, Mims CW, Westcott SWI. 1992. Ultrastructure of root cortical cells parasitized by the ring nematode Criconemella xenoplax. Protoplasma 167:55-65
61. Iberkleid I, Vieira P, de Almeida Engler J, Firester K, Spiegel Y, Horowitz SB. 2013. Fatty acid- and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes. PLoS ONE 8:e64586
62. Ithal N, Recknor J, Nettleton D, Hearne L, Maier T, 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
63. Jaouannet M, Magliano M, Arguel MJ, Gourgues M, Evangelisti E, 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
64. Jasmer DP, Goverse A, Smant G. 2003. Parasitic nematode interactions with mammals and plants. Annu. Rev. Phytopathol. 41:245-70
65. Jaubert S, Ledger TN, Laffaire JB, Piotte C, Abad P, Rosso MN. 2002. Direct identification of stylet secreted proteins from root-knot nematodes by a proteomic approach. Mol. Biochem. Parasitol. 121:205-11
66. Jaubert S, Milac AL, Petrescu AJ, de Almeida-Engler J, Abad P, Rosso MN. 2005. In planta secretion of a calreticulin by migratory and sedentary stages of root-knot nematode. Mol. Plant-Microbe Interact. 18:1277-84
67. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323-29
68. Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, et al. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Mol. Plant Pathol. 14:946-61
69. Jones JT, Kumar A, Pylypenko LA, Thirugnanasambandam A, Castelli L, 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
70. Jones JT, Reavy B, Smant G, Prior AE. 2004. Glutathione peroxidases of the potato cyst nematode Globodera rostochiensis. Gene 324:47-54
71. Jones MGK, Northcote DH. 1972. Nematode-induced syncytium: a multinucleate transfer cell. J. Cell Sci. 10:789-809
72. Kandoth PK, Ithal N, Recknor J, Maier T, Nettleton D, 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
73. Kandoth PK, Mitchum MG. 2013. War of the worms: how plants flight underground attacks. Curr. Opin. Plant Biol. 16:457-63
74. Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S. 2004. Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stressregulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol. 45:712-22
75. Khallouk S, Voisin R, Van Ghelder C, Engler G, Amiri S, Esmenjaud D. 2011. Histological mechanisms of the resistance conferred by the Ma gene against Meloidogyne incognita in Prunus spp. Phytopathology 101:945-51
76. Koropacka K. 2010. Molecular contest between potato and potato cyst nematode Globodera pallida: modulation of Gpa2-mediated resistance. PhD Thesis, Wageningen Univ., Wageningen. 132 pp.
77. Kouassi AB, Kerlan MC, Sobczak M, Dantec JP, Rouaux C, et al. 2004. Resistance to the root-knot nematode Meloidogyne fallax in Solanum sparsipilum: analysis of the mechanisms. Nematology 6:389-400
78. Kruger J, Thomas CM, Golstein C, Dixon MS, Smoker M, et al. 2002. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296:744-47
79. Kyndt T, Vieira P, Gheysen G, de Almeida-Engler J. 2013. Nematode feeding sites: unique organs in plant roots. Planta 238:807-18
80. Lambert KN, Ferrie BJ, Nombela G, Brenner ED, Williamson VM. 1999. Identification of genes whose transcripts accumulate rapidly in tomato after root-knot nematode infection. Physiol. Mol. Plant Pathol. 55:341-48
81. Lecourieux D, Ranjeva R, Pugin A. 2006. Calcium in plant defence-signalling pathways. New Phytol. 171:249-69
82. Li Q, Xie QG, Smith-Becker J, Navarre DA, Kaloshian I. 2006. Mi-1-mediated aphid resistance involves salicylic acid andmitogen-activated protein kinase signaling cascades. Mol. Plant-Microbe Interact. 19:655-64
83. Li X, Zhuo K, Luo M, Sun L, Liao J. 2011. Molecular cloning and characterization of a calreticulin cDNA from the pinewood nematode Bursaphelenchus xylophilus. Exp. Parasitol. 128:121-26
84. Li Z, Liu X, Chu Y, Wang Y, Zhang Q, Zhou X. 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
85. Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R, et al. 2012. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492:256-60
86. Lozano-Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Finkers-Tomczak A, 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
87. Lukasik-Shreepaathy E, Slootweg E, Richter H, Goverse A, Cornelissen BJC, Takken FLW. 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
88. Mahalingam R, Skorupska HT. 1996. Cytological expression of early response to infection by Heterodera glycines Ichinohe in resistant PI 437654 soybean. Genome 39:986-98
89. Mantelin S, Peng HC, Li B, Atamian HS, Takken FLW, Kaloshian I. 2011. The receptor-like kinase SlSERK1 is required for Mi-1-mediated resistance to potato aphids in tomato. Plant J. 67:459-71
90. Martinez de Ilarduya O, Nombela G, Hwang CF, Williamson VM, Muniz M, Kaloshian I. 2004. Rme1 is necessary for Mi-1-mediated resistance and acts early in the resistance pathway. Mol. Plant-Microbe Interact. 17:55-61
91. Matsye PD, Lawrence GW, Youssef RM, Kim KH, Lawrence KS, et al. 2012. The expression of a naturally occurring, truncated allele of an-SNAP gene suppresses plant parasitic nematode infection. Plant Mol. Biol. 80:131-55
92. Melillo MT, Leonetti P, Bongiovanni M, Castagnone-Sereno P, Bleve-Zacheo T. 2006. Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomatoroot- knot nematode interactions. New Phytol. 170:501-12
93. Melillo MT, Leonetti P, Leone A, Veronico P, Bleve-Zacheo T. 2011. ROS and NO production in compatible and incompatible tomato-Meloidogyne incognita interactions. Eur. J. Plant Pathol. 130:489-502
94. Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM. 1998. The root knot nematode resistance gene Mi from tomato is amember of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307-19
95. Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA, et al. 2013. Nematode effector proteins: an emerging paradigm of parasitism. New Phytol. 199:879-94
96. Monaghan J, Zipfel C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:349-57
97. Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA. 2008. Plant polyamine catabolism: the state of the art. Plant Signal. Behav. 3:1061-66
98. Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596-601
99. Mylonas C, Kouretas D. 1999. Lipid peroxidation and tissue damage. In Vivo 13:295-309
100. Neher DA. 2010. Ecology of plant and free-living nematodes in natural and agricultural soil. Annu. Rev. Phytopathol. 48:371-94
101. Nishimura MT, Dangl JL. 2010. Arabidopsis and the plant immune system. Plant J. 61:1053-66
102. Nombela G, Williamson VM, Muniz M. 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
103. Offler CE, McCurdy DW, Patrick JW, Talbot MJ. 2003. Transfer cells: cells specialized for a special purpose. Annu. Rev. Plant Biol. 54:431-54
104. Paal J, Henselewski H, Muth J, Meksem K, Menendez CM, 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
105. Patel N, Hamamouch N, Li C, Hewezi T, Hussey RS, et al. 2010. A nematode effector protein similar to annexins in host plants. J. Exp. Bot. 61:235-48
106. 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. 2:227-34
107. Peng H, Gao BL, Kong LA, YuQ, Huang WK, et al. 2013. Exploring the host parasitism of themigratory plant-parasitic nematode Ditylenchus destructor by expressed sequence tags analysis. PLoS ONE 8:e69579
108. Perry RN. 1989. Dormancy and hatching of nematode eggs. Parasitol. Today 5:377-83
109. Postma WJ, Slootweg EJ, Rehman S, Finkers-Tomczak A, Tytgat TO, et al. 2012. The effector SPRYSEC-19 of Globodera rostochiensis suppresses CC-NB-LRR-mediated disease resistance in plants. Plant Physiol. 160:944-54
110. Prior A, Jones JT, Blok VC, Beauchamp J, McDermott L, 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
111. Rairdan GJ, Moffett P. 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
112. Ramrez V, L opez A, Mauch-Mani B, Gil MJ, Vera P. 2013. An extracellular subtilase switch for immune priming in Arabidopsis. PLoS Pathog. 9:e1603445
113. Rehman S, Butterbach P, Popeijus H, Overmars H, Davis EL, et al. 2009. Identification and characterization of the most abundant cellulases in stylet secretions from Globodera rostochiensis. Phytopathology 99:194-202
114. Rehman S, Postma W, Tytgat T, Prins P, Qin L, et al. 2009. A secreted SPRY domain-containing protein (SPRYSEC) from the plant-parasitic nematode Globodera rostochiensis interacts with a CC-NBLRR protein from a susceptible tomato. Mol. Plant-Microbe Interact. 22:330-40
115. Reinbothe C, Springer A, Samol I, Reinbothe S. 2009. Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence. FEBS J. 276:4666-81
116. 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 geneH1derived from Solanum tuberosum ssp. andigena. Physiol. Mol. Plant Pathol. 27:219-34
117. Robertson L, Robertson WM, Sobczak M, Helder J, Tetaud E, et al. 2000. Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis. Mol. Biochem. Parasitol. 111:41-49
118. Rooney HC, Van't Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, de Wit PJ. 2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783-86
119. Sacco MA, Koropacka K, Grenier E, Jaubert MJ, Blanchard A, et al. 2009. The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathog. 5:e1000564
120. Schulz P, Herde M, Romeis T. 2013. Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol. 163:523-30
121. Schwessinger B, Zipfel C. 2008. News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 11:389-95
122. Sheridan JP, Miller AJ, Perry RN. 2004. Early responses of resistant and susceptible potato roots during invasion by the potato cyst nematode Globodera rostochiensis. J. Exp. Bot. 55:751-60
123. Sijmons PC, Atkinson HJ, Wyss U. 1994. Parasitic strategies of root nematodes and associated host cell responses. Annu. Rev. Phytopathol. 32:235-59
124. Slootweg EJ, Spiridon LN, Roosien J, Butterbach P, Pomp R, 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
125. Sobczak M, Avrova A, Jupowicz J, Phillips MS, Ernst K, Kumar A. 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
126. Takken FLW, Goverse A. 2012. How to build a pathogen detector: structural basis ofNB-LRR function. Curr. Opin. Plant Biol. 15:375-84
127. Tameling WIL, Elzinga SDJ, Darmin PS, Vossen JH, Takken FLW, 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
128. Tang L, Smith VP, Gounaris K, Selkirk ME. 1996. Brugia pahangi: the cuticular glutathione peroxidase (gp29) protects heterologous membranes from lipid peroxidation. Exp. Parasitol. 82:329-32
129. Thomma BPHJ, Nurnberger T, Joosten MHAJ. 2011. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4-15
130. Torres MA, Jones JDG, Dangl JL. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141:373-78
131. Trudgill DL. 1967. The effect of environment on sex determination in Heterodera rostochiensis. Nematologica 13:263-72
132. Turk B, Turk D, Turk V. 2012. Protease signalling: the cutting edge. EMBO J. 31:1630-43
133. Tytgat T, Vanholme B, De Meutter J, Claeys M, Couvreur M, 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
134. van der Hoorn RA, Jones JD. 2004. The plant proteolytic machinery and its role in defence. Curr. Opin. Plant Biol. 7:400-7
135. van der Hoorn RA, Kamoun S. 2008. From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009-17
136. van der Vossen EAG, van der Voort JNAM, Kanyuka K, Bendahmane A, Sandbrink H, 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
137. van Esse HP, Van't Klooster JW, Bolton MD, Yadeta KA, van Baarlen P, et al. 2008. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20:1948-63
138. Van Loon LC, Rep M, Pieterse CMJ. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135-62
139. van Megen H, van den Elsen S, Holterman M, Karssen G, Mooyman P, et al. 2009. A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927-50
140. Vieira P, Escudero C, Rodiuc N, Boruc J, Russinova E, et al. 2013. Ectopic expression of Kip-related proteins restrains root-knot nematode-feeding site expansion. New Phytol. 199:505-19
141. Vieira P, Kyndt T, Gheysen G, de Almeida Engler J. 2013. An insight into critical endocycle genes for plant-parasitic nematode feeding sites establishment. Plant Signal. Behav. 8:e242231
142. Vierstra RD. 2009. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10:385-97
143. Vos C, Van den Broucke D, Lombi FM, DeWaele D, Elsen A. 2012. Mycorrhiza-induced resistance in banana acts on nematode host location and penetration. Soil Biol. Biochem. 47:60-66
144. Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, et al. 1998. The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat. Biotechnol. 16:1365
145. 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 1:681-86
146. Williamson VM, Hussey RS. 1996. Nematode pathogenesis and resistance in plants. Plant Cell 8:1735-45
147. Williamson VM, Kumar A. 2006. Nematode resistance in plants: the battle underground. Trends Genet. 22:396-403
148. Woo JS, Imm JH, Min CK, Kim KJ, Cha SS, Oh BH. 2006. Structural and functional insights into the B30.2/SPRY domain. EMBO J. 25:1353-63
149. Wubben MJE II, Su H, Rodermel SR, Baum TJ. 2001. Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 14:1206-12
150. Wyss U, Grundler FMW. 1992. Feeding behaviour of sedentary plant parasitic nematodes. Neth. J. Plant Pathol. 98(Suppl. 2):165-73
151. Zunke U. 1990. Observations on the invasion and endoparasitic behaviour of the root lesion nematode Pratylenchus penetrans. J. Nematol. 22:309-20