, Volume 238, Issue 5, pp 807–818 | Cite as

Nematode feeding sites: unique organs in plant roots



Although generally unnoticed, nearly all crop plants have one or more species of nematodes that feed on their roots, frequently causing tremendous yield losses. The group of sedentary nematodes, which are among the most damaging plant-parasitic nematodes, cause the formation of special organs called nematode feeding sites (NFS) in the root tissue. In this review we discuss key metabolic and cellular changes correlated with NFS development, and similarities and discrepancies between different types of NFS are highlighted.


Sedentary nematode Giant cell Syncytium Phytohormones 


  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 13:47PubMedCrossRefGoogle Scholar
  2. Banora MY, Rodiuc N, Baldacci-Cresp F, Smertenko A, Bleve-Zacheo T, Mellilo MT, Karimi M, Hilson P, Evrard JL, Favery B, Engler G, Abad P, de Almeida Engler J (2011) Feeding cells induced by phytoparasitic nematodes require γ-tubulin ring complex for microtubule reorganization. PLoS Pathog 7:e1002343PubMedCrossRefGoogle Scholar
  3. Barcala M, Garcia A, Cabrera J, Casson S, Lindsey K, Favery B, Garcia-Casado G, Solano R, Fenoll C, Escobar C (2010) Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J 61:698–712PubMedCrossRefGoogle Scholar
  4. Bockenhoff A (1995) Untersuchungen zur physiologie der nährstoffversorgung des rübenzystennematoden Heterodera schachtii und der von ihm induzierten nährzellen in wurzeln von Arabidopsis thaliana unter verwendung einer speziell adaptierten in situ mikroinjektionstechnik. PhD thesis, University of Kiel, GermanyGoogle Scholar
  5. Bockenhoff A, Prior DAM, Grundler FMW, Oparka KJ (1996) Induction of phloem unloading in Arabidopsis thaliana roots by the parasitic nematode Heterodera schachtii. Plant Physiol 112:1421–1427PubMedCrossRefGoogle Scholar
  6. Caillaud M-C, Lecomte P, Jammes F, Quenton M, Pagnotta S, Andrio E, de Almeida Engler J, Marfaing N, Gounon P, Abad P, Favery B (2008) MAP65 microtubule-associated protein is essential for nematode-induced giant cell ontogenesis in Arabidopsis. Plant Cell 20:423–437PubMedCrossRefGoogle Scholar
  7. Campbell P, Braam J (1999) Xyloglucan endotransglycosylases: diversity of genes, enzymes and potential wall-modifying functions. Trends Plant Sci 4:361–366PubMedCrossRefGoogle Scholar
  8. Chapman EJ, Estelle M (2009) Cytokinin and auxin intersection in root meristems. Genome Biol 10Google Scholar
  9. Churchman ML, Brown ML, Kato N, Kirik V, Hülskamp M, Inzé D, De Veylder L, Walker JD, Zheng Z, Oppenheimer DG, Gwin T, Churchman J, Larkin JC (2006) SIAMESE, a novel plant-specific cell cycle regulator controls endoreplication onset in Arabidopsis thaliana. Plant Cell 18:3145–3157PubMedCrossRefGoogle Scholar
  10. Clément A, Ketelaar T, Rodiuc N, Banora MY, Smertenko A, Engler G, Abad P, Hussey PJ, de Almeida Engler J (2009) Actin-depolymerizing factor2-mediated actin dynamics are essential for root-knot nematode infection in Arabidopsis. Plant Cell 21:2963–2979PubMedCrossRefGoogle Scholar
  11. de Almeida Engler J, Favery B (2011) The plant cytoskeleton remodelling in nematode induced feeding sites. In: Jones J, Gheysen G, Fenoll C (eds) Genomics and molecular genetics of plant-nematode interactions. Springer Science + Business Media, Dordrecht, The Netherlands, pp 369–394Google Scholar
  12. de Almeida Engler J, Gheysen G (2013) Nematode-induced endoreduplication in plant host cells: why and how? Mol Plant Microbe Interact 26:17–24PubMedCrossRefGoogle Scholar
  13. de Almeida Engler J, De Vleesschauwer V, Burssens S, Celenza JLJ, Inzé D, Van Montagu M, Engler G, Gheysen G (1999) Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Cell 11:793–808PubMedGoogle Scholar
  14. de Almeida Engler J, Van Poucke K, Karimi M, De Groodt R, Gheysen G, Engler G, Gheysen G (2004) Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. Plant J 38:12–26PubMedCrossRefGoogle Scholar
  15. de Almeida Engler J, Engler G, Gheysen G (2011) Unravelling the plant cell cycle in nematode induced feeding sites. In: Jones J, Gheysen G, Fenoll C (eds) Genomics and molecular genetics of plant-nematode interactions. Springer Science + Business Media, Dordrecht, The Netherlands, pp 349–368Google Scholar
  16. de Almeida Engler J, Kyndt T, Vieira P, Van Cappelle E, Bouldolf V, Sanchez V, Escobar C, De Veylder L, Engler G, Abad P, Gheysen G (2012) CCS52 and DEL1 genes are key components of the endocycle in nematode induced feeding sites. Plant J 72:185–198PubMedCrossRefGoogle Scholar
  17. De Smet I, Lau S, Voss U, Vanneste S, Benjamins R, Rademacher EH, Schlereth A, De Rybel B, Vassileva V, Grunewald W, Naudts M, Levesque MP, Ehrismann JS, Inze D, Luschnig C, Benfey PN, Weijers D, Van Montagu MCE, Bennett MJ, Jurgens G, Beeckman T (2010) Bimodular auxin response controls organogenesis in Arabidopsis. Proc Natl Acad Sci USA 107:2705–2710PubMedCrossRefGoogle Scholar
  18. Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17:678–682PubMedCrossRefGoogle Scholar
  19. Dorhout R, Gommers FJ, Kolloffel C (1993) Phloem transport of carboxyfluorescein through tomato roots infected with Meloidogyne incognita. Physiol Mol Plant Pathol 43:1–10CrossRefGoogle Scholar
  20. Eklöf JM, Brumer H (2010) The XTH gene family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiol 153:456–466PubMedCrossRefGoogle Scholar
  21. Favery B, Complainville A, Vinardell JM, Lecomte P, Vaubert D, Mergaert P, Kondorosi A, Kondorosi E, Crespi M, Abad P (2002) The endosymbiosis-induced genes ENOD40 and CCS52a are involved in endoparasitic-nematode interactions in Medicago truncatula. Mol Plant Microbe Interact 15:1008–1013PubMedCrossRefGoogle Scholar
  22. 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 26:75–86PubMedCrossRefGoogle Scholar
  23. Gheysen G, Fenoll C (2002) Gene expression in nematode feeding sites. Annu Rev Phytopathol 40:191–219PubMedCrossRefGoogle Scholar
  24. Gheysen G, Mitchum MG (2009) Molecular insights in the susceptible plant response to nematode infection. Plant Cell Monogram 15:45–81CrossRefGoogle Scholar
  25. Glazer I, Orion D, Apelbaum A (1983) Interrelationships between ethylene production, gall formation, and root-knot nematode development in tomato plants infected with Meloidogyne-javanica. J Nematol 15:539–544Google Scholar
  26. Glazer I, Apelbaum A, Orion D (1985) Effect of inhitbitors and stimulators of ethylene production on gall development in Meloidogyne-javanica-infected tomato roots. J Nematol 17:145–149PubMedGoogle Scholar
  27. Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder J (2000) Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Mol Plant Microbe Interact 13:1121–1129PubMedCrossRefGoogle Scholar
  28. Grundler FMW, Sobczak M, Golinowski W (1998) Formation of wall openings in root cells of Arabidopsis thaliana following infection by the plant-parasitic nematode Heterodera schachtii. Eur J Plant Pathol 104:545–551CrossRefGoogle Scholar
  29. Grunewald W, Cannoot B, Friml J, Gheysen G (2009a) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog 5:e1000266PubMedCrossRefGoogle Scholar
  30. Grunewald W, van Noorden G, van Isterdael G, Beeckman T, Gheysen G, Mathesius U (2009b) Manipulation of auxin transport in plant roots during Rhizobium symbiosis and nematode parasitism. Plant Cell 21:2553–2562PubMedCrossRefGoogle Scholar
  31. Haegeman A, Mantelin S, Jones JT, Gheysen G (2012) Functional roles of effectors of plant-parasitic nematodes. Gene 492:19–31PubMedCrossRefGoogle Scholar
  32. Hamamouch N, Li CY, Seo PJ, Park CM, Davis EL (2011) Expression of Arabidopsis pathogenesis-related genes during nematode infection. Mol Plant Pathol 12:355–364PubMedCrossRefGoogle Scholar
  33. Hammes UZ, Schachtman DP, Berg RH, Nielsen E, Koch W, McIntyre LM, Taylor CG (2005) Nematode-induced changes of transporter gene expression in Arabidopsis roots. Mol Plant Microbe Interact 18:1247–1257PubMedCrossRefGoogle Scholar
  34. Hermsmeier D, Hart JK, Byzova M, Rodermel SR, Baum TJ (2000) Changes in mRNA abundance within Heterodera schachtii-infected roots of Arabidopsis thaliana. Mol Plant Microbe Interact 13:309–315PubMedCrossRefGoogle Scholar
  35. Hewezi T, Howe P, Maier TR, Baum TJ (2008) Arabidopsis small RNAs and their targets during cyst nematode parasitism. Mol Plant Microbe Interact 21:1622–1634PubMedCrossRefGoogle Scholar
  36. Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (2010) Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol 152:968–984PubMedCrossRefGoogle Scholar
  37. Hewezi T, Maier TR, Nettleton D, Baum TJ (2012) The Arabidopsis microRNA396-GRF1/GRF3 regulatory module acts as a developmental regulator in the reprogramming of root cells during cyst nematode infection. Plant Physiol 159:321–335PubMedCrossRefGoogle Scholar
  38. Hofmann J, Grundler FMW (2006) Females and males of root-parasitic cyst nematodes induce different symplasmic connections between their syncytial feeding cells and the phloem in Arabidopsis thaliana. Plant Physiol Biochem 44:430–433PubMedCrossRefGoogle Scholar
  39. Hofmann J, Wieczorek K, Blochl A, Grundler FMW (2007) Sucrose supply to nematode-induced syncytia depends on the apoplasmic and symplasmic pathways. J Exp Bot 58:1591–1601PubMedCrossRefGoogle Scholar
  40. Hofmann J, Szakasits D, Blochl A, Sobczak M, Daxbock-Horvath S, Golinowski W, Bohlmann H, Grundler FMW (2008) Starch serves as carbohydrate storage in nematode-induced syncytia. Plant Physiol 146:228–235PubMedCrossRefGoogle Scholar
  41. Hofmann J, El Ashry A, Anwar S, Erban A, Kopka J, Grundler F (2010) Metabolic profiling reveals local and systemic responses of host plants to nematode parasitism. Plant J 62:1058–1071PubMedGoogle Scholar
  42. Hoth S, Schneidereit A, Lauterbach C, Scholz-Starke J, Sauer N (2005) Nematode infection triggers the de novo formation of unloading phloem that allows macromolecular trafficking of green fluorescent protein into syncytia. Plant Physiol 138:383–392PubMedCrossRefGoogle Scholar
  43. Hoth S, Stadler R, Sauer N, Hammes UZ (2008) Differential vascularization of nematode-induced feeding sites. Proc Natl Acad Sci USA 105:12617–12622PubMedCrossRefGoogle Scholar
  44. Huang CS, Maggenti AR (1969) Wall modifications in developing giant cells of Vicia faba and Cucumis sativus induced by root knot nematode, Meloidogyne javanica. Phytopathology 59:931–937PubMedGoogle Scholar
  45. Hudson LC (2008) Analysis of cell wall synthesis genes in feeding cells formed by root-knot nematodes. PhD Dissertation, North Carolina State UniversityGoogle Scholar
  46. Hutangura P, Mathesius U, Jones MGK, Rolfe BG (1999) Auxin induction is a trigger for root gall formation caused by root-knot nematodes in white clover and is associated with the activation of the flavonoid pathway. Aust J Plant Physiol 26:221–231CrossRefGoogle Scholar
  47. Ibrahim HMM, Hosseini P, Alkharouf NW, Hussein EHA, El-Din AYG, Aly MAM, Matthews BF (2011) Analysis of gene expression in soybean (Glycine max) roots in response to the root knot nematode Meloidogyne incognita using microarrays and KEGG pathways. BMC Genomics 12:220PubMedCrossRefGoogle Scholar
  48. Inzé D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40:77–105PubMedCrossRefGoogle Scholar
  49. Ithal N, Recknor J, Nettleton D, Hearne L, Maier T, Baum TJ, Mitchum MG (2007a) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol Plant Microbe Interact 20:293–305PubMedCrossRefGoogle Scholar
  50. Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG (2007b) Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol Plant Microbe Interact 20:510–525PubMedCrossRefGoogle Scholar
  51. Jammes F, Lecomte P, Almeida-Engler J, Bitton F, Martin-Magniette ML, Renou JP, Abad P, Favery B (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant J 44:447–458PubMedCrossRefGoogle Scholar
  52. Ji H, Gheysen G, Denil S, Lindsey K, Topping JF, Nahar K, Haegeman A, De Vos WH, Trooskens G, Van Criekinge W, De Meyer T, Kyndt T (in press) Transcriptional analysis through RNA sequencing of giant cells induced by Meloidogyne graminicola in rice roots. J Exp BotGoogle Scholar
  53. Karczmarek A, Overmars H, Helder J, Goverse A (2004) Feeding cell development by cyst and root-knot nematodes involves a similar early, local and transient activation of a specific auxin-inducible promoter element. Mol Plant Pathol 5:343–346PubMedCrossRefGoogle Scholar
  54. Katsir L, Davies KA, Bergmann DC, Laux T (2011) Peptide signaling in plant development. Curr Biol 21:R356–R364PubMedCrossRefGoogle Scholar
  55. Klink VP, Overall CC, Alkharouf NW, MacDonald MH, Matthews BF (2007) Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean (Glycine max) roots infected by the soybean cyst nematode (Heterodera glycines). Planta 226:1389–1409PubMedCrossRefGoogle Scholar
  56. Kobayashi K, Baba S, Obayashi T, Sato M, Toyooka K, Keranen M, Aro EM, Fukaki H, Ohta H, Sugimoto K, Masuda T (2012) Regulation of root greening by light and auxin/cytokinin signaling in Arabidopsis. Plant Cell 24:1081–1095PubMedCrossRefGoogle Scholar
  57. Koltai H, Dhandaydham M, Opperman C, Thomas J, Bird D (2001) Overlapping plant signal transduction pathways induced by a parasitic nematode and a rhizobial endosymbiont. Mol Plant Microbe Interact 14:1168–1177PubMedCrossRefGoogle Scholar
  58. Kyndt T, Denil S, Haegeman A, Trooskens G, Bauters L, Van Criekinge W, De Meyer T, Gheysen G (2012a) Transcriptional reprogramming by root knot and migratory nematode infection in rice. New Phytol 196:887–900PubMedCrossRefGoogle Scholar
  59. Kyndt T, Nahar K, Haegeman A, De Vleesschauwer D, Hofte M, Gheysen G (2012b) Comparing systemic defence-related gene expression changes upon migratory and sedentary nematode attack in rice. Plant Biol 14:73–82PubMedCrossRefGoogle Scholar
  60. Lee C, Chronis D, Kenning C, Peret B, Hewezi T, Davis EL, Baum TJ, Hussey R, Bennett M, Mitchum MG (2011) The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiol 155:866–880PubMedCrossRefGoogle Scholar
  61. Li X, Wang X, Zhang S, Liu D, Duan Y, Dong W (2012) Identification of soybean microRNAs involved in soybean cyst nematode infection by deep sequencing. PLoS One 7(6):e39650PubMedCrossRefGoogle Scholar
  62. Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM (2004) Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J 38:203–214PubMedCrossRefGoogle Scholar
  63. Lu SW, Chen S, Wang J, Yu H, Chronis D, Mitchum MG, Wang X (2009) Structural and functional diversity of CLAVATA3/ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis. Mol Plant Microbe Interact 22:1128–1142PubMedCrossRefGoogle Scholar
  64. Mazarei M, Puthoff DP, Hart JK, Rodermel SR, Baum TJ (2002) Identification and characterization of a soybean ethylene-responsive element-binding protein gene whose mRNA expression changes during soybean cyst nematode infection. Mol Plant Microbe Interact 15:577–586PubMedCrossRefGoogle Scholar
  65. Mazarei M, Lennon KA, Puthoff DP, Rodermel SR, Baum TJ (2003) Expression of an Arabidopsis phosphoglycerate mutase homologue is localized to apical meristems, regulated by hormones, and induced by sedentary plant-parasitic nematodes. Plant Mol Biol 53:513–530PubMedCrossRefGoogle Scholar
  66. 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 tomato-root-knot nematode interactions. New Phytol 170:501–512PubMedCrossRefGoogle Scholar
  67. Nahar K, Kyndt T, De Vleesschauwer D, Hofte M, Gheysen G (2011) The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol 157:305–316PubMedCrossRefGoogle Scholar
  68. Nahar K, Kyndt T, Hause B, Hofte M, Gheysen G (2013) Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway. Mol Plant Microbe Interact 26:106–115PubMedCrossRefGoogle Scholar
  69. Niebel A, de Almeida Engler J, Hemerly A, Ferreira P, Van Montagu M, Gheysen G (1996) Induction of cdc2a and cyc1At expression in Arabidopsis during early phases of nematode-induced feeding cell formation. Plant J 10:1037–1043PubMedCrossRefGoogle Scholar
  70. Opperman CH, Taylor CG, Conkling MA (1994) Root-knot nematode-directed expression of a plant root-specific gene. Science 263:221–223PubMedCrossRefGoogle Scholar
  71. Portillo M, Cabrera J, Lindsey K, Topping J, Andrés MF, Emiliozzi M, Oliveros JC, García-Casado G, Solano R, Koltai H, Resnick N, Fenoll C, Escobar C (2013) Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: a functional role for gene repression. New Phytol 197:1276–1290PubMedCrossRefGoogle Scholar
  72. Replogle A, Wang J, Bleckmann A, Hussey R, Baum T, Sawa S, Davis EL, Wang X, Simon R, Mitchum MG (2011) Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. Plant J 65:430–440PubMedCrossRefGoogle Scholar
  73. Richards DE, King KE, Ait-ali T, Harberd NP (2001) How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling. Ann Rev Plant Physiol Plant Mole Biol 52:67–88CrossRefGoogle Scholar
  74. Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343PubMedCrossRefGoogle Scholar
  75. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289PubMedCrossRefGoogle Scholar
  76. Starr JL (1993) Dynamics of the nuclear complement of giant cells induced by Meloidogyne incognita. J Nematol 25:416–421PubMedGoogle Scholar
  77. Strader LC, Chen GL, Bartel B (2010) Ethylene directs auxin to control root cell expansion. Plant J 64:874–884PubMedCrossRefGoogle Scholar
  78. Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GTS, Sandberg G, Bhalerao R, Ljung K, Bennett MJ (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196PubMedCrossRefGoogle Scholar
  79. Szakasits D, Heinen P, Wieczorek K, Hofmann J, Wagner F, Kreil DP, Sykacek P, Grundler FMW, Bohlmann H (2009) The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant J 57:771–784PubMedCrossRefGoogle Scholar
  80. Trehin C, Planchais S, Glab N, Perennes C, Tregear J, Bergounioux C (1998) Cell cycle regulation by plant growth regulators: involvement of auxin and cytokinin in the re-entry of Petunia protoplasts into the cell cycle. Planta 206:215–224PubMedCrossRefGoogle Scholar
  81. Verkest A, Weinl C, Inzé D, De Veylder L, Schnittger A (2005) Switching the cell cycle. Kip-related proteins in plant cell cycle control. Plant Physiol 139:1099–1106PubMedCrossRefGoogle Scholar
  82. Vieira P, Engler G, de Almeida Engler J (2012a) Whole-mount confocal imaging of nuclei in giant feeding-cells induced by root-knot nematodes in Arabidopsis. New Phytol 195:488–496PubMedCrossRefGoogle Scholar
  83. Vieira P, Youssef M, Castagnone-Sereno P, Rosso M-N, Engler G, de Almeida Engler J (2012b) An immunocytochemical procedure for protein localization in nematode pre-parasitic and parasitic stages using methylacrylate-embedded tissues. Phytopathology 102:990–996PubMedCrossRefGoogle Scholar
  84. Vieira P, Escudero C, Rodiuc N, Boruc J, Russinova E, Glab N, Mota M, De Veylder L, Abad P, Engler G, de Almeida Engler J (2013) Ectopic expression of kip-related proteins restrains root-knot nematode-feeding site expansion. New Phytol (in press)Google Scholar
  85. Vinardell JM, Fedorova E, Cebolla A, Kevei Z, Hovarth G, Kelemen Z, Tarayre S, Roudier F, Mergaert P, Kondorosi A, Kondorosi E (2003) Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 15:2093–2105PubMedCrossRefGoogle Scholar
  86. Wang J, Lee C, Replogle A, Joshi S, Korkin D, Hussey R, Baum TJ, Davis EL, Wang X, Mitchum MG (2010) Dual roles for the variable domain in protein 20 trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytol 187:1003–1017PubMedCrossRefGoogle Scholar
  87. Wang J, Replogle A, Hussey R, Baum T, Wang X, Davis EL, Mitchum MG (2011) Identification of potential host plant mimics of CLV3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii. Mol Plant Pathol 12:177–186PubMedCrossRefGoogle Scholar
  88. Wieczorek K, Golecki B, Gerdes L, Heinen P, Szakasits D, Durachko DM, Cosgrove DJ, Kreil DP, Puzio PS, Bohlmann H, Grundler FMW (2006) Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana. Plant J 48:98–112PubMedCrossRefGoogle Scholar
  89. Wieczorek K, Hofmann J, Blochl A, Szakasits D, Bohlmann H, Grundler FMW (2008) Arabidopsis endo-1,4-beta-glucanases are involved in the formation of root syncytia induced by Heterodera schachtii. Plant J 53:336–351PubMedCrossRefGoogle Scholar
  90. Wiggers RJ, Starr JL, Price HJ (1990) DNA content and variation in chromosome number in plant cells affected by Meloidogyne incognita and M. arenaria. Phytopathology 80:1391–1395CrossRefGoogle Scholar
  91. Wolf S, Mravec J, Greiner S, Mouille G, Hofte H (2012) Plant cell wall homeostasis is mediated by brassinosteroid feedback signaling. Curr Biol 22:1732–1737PubMedCrossRefGoogle Scholar
  92. Wubben MJE, 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 14:1206–1212PubMedCrossRefGoogle Scholar
  93. Wubben MJE, Jin J, Baum TJ (2008) Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Mol Plant Microbe Interact 21:424–432PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department Molecular BiotechnologyGhent University (UGent)GhentBelgium
  2. 2.Institut National de la Recherche Agronomique, UMR 1355 ISA, Centre National de la Recherche ScientifiqueUMR 7254 ISA, Université de Nice-Sophia Antipolis, UMR ISASophia-AntipolisFrance
  3. 3.NemaLab, ICAAM, Instituto de Ciências Agrárias e Ambientais MediterrânicasUniversidade de ÉvoraÉvoraPortugal

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