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Compatible Plant-Root Knot Nematode Interaction and Parallels with Symbiosis

  • Bruno Favery
  • Michaël Quentin
  • Pierre AbadEmail author
Chapter
  • 1.4k Downloads
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 11)

Abstract

Among plant pathogens, the root-knot nematodes (RKN), Meloidogyne spp., are obligate biotrophic pathogens that can establish and maintain an intimate relationship with their host plants. They are able to induce the redifferentiation of root cells into hypertrophied and multinucleate feeding cells essential for their development. Hyperplasia of the surrounding feeding cells lead to the organogenesis of a typical root gall. In this chapter, we describe the complex interactions between RKN and their infected hosts. We highlight the progress in our understanding of host plant response during the compatible interaction focusing on key plant functions involved in giant cell ontogenesis. Throughout, parallels with symbiotic rhizobia–legume interactions are emphasized.

Keywords

Giant Cell Auxin Transport Gall Formation Root Gall Giant Cell Formation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abad P, Williamson VM (2010) Plant nematode interaction: a sophisticated dialogue. In: Kader J-C, Delseny M (eds) Advances in botanical research. Academic, New York, pp 147–192Google Scholar
  2. Abramovitch RB, Martin GB (2004) Strategies used by bacterial pathogens to suppress plant defenses. Curr Opin Plant Biol 7:356–364PubMedCrossRefGoogle Scholar
  3. Anderson JP, Lichtenzveig J, Gleason C, Oliver RP, Singh KB (2010) The B-3 ethylene response factor MtERF1-1 mediates resistance to a subset of root pathogens in Medicago truncatula without adversely affecting symbiosis with rhizobia. Plant Physiol 154:861–873PubMedCentralPubMedCrossRefGoogle Scholar
  4. Barcala M, Garcia A, Cubas P, Almoguera C, Jordano J, Fenoll C, Escobar C (2008) Distinct heat-shock element arrangements that mediate the heat shock, but not the late-embryogenesis induction of small heat-shock proteins, correlate with promoter activation in root-knot nematode feeding cells. Plant Mol Biol 66:151–164PubMedCrossRefGoogle Scholar
  5. 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
  6. Bar-Orl C, Kapulnik Y, Koltai H (2005) A broad characterization of the transcriptional profile of the compatible tomato response to the plant parasitic root knot nematode Meloidogyne javanica. Eur J Plant Pathol 111:181–192CrossRefGoogle Scholar
  7. Barthels N, Van der Lee FM, Klap J, Goddijn OJM, Karimi M, Puzio P, Grundler FMW, Ohl SA, Lindsey K, Robertson VM, Van Montagu M, Gheysen G, Sijmons PC (1997) Regulatory sequences of Arabidopsis drive reporter gene expression in nematode feeding structures. Plant Cell 9:2119–2134PubMedCentralPubMedGoogle Scholar
  8. Bartsev AV, Deakin WJ, Boukli NM, McAlvin CB, Stacey G, Malnoe P, Broughton WJ, Staehelin C (2004) NopL, an effector protein of Rhizobium sp. NGR234, thwarts activation of plant defense reactions. Plant Physiol 134:871–879PubMedCentralPubMedCrossRefGoogle Scholar
  9. Bhattarai KK, Xie QG, Mantelin S, Bishnoi U, Girke T, Navarre DA, Kaloshian I (2008) Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Mol Plant Microbe Interact 21:1205–1214PubMedCrossRefGoogle Scholar
  10. Bird DM, Kaloshian I (2003) Are roots special? Nematodes have their say. Physiol Mol Plant Pathol 62:115–123CrossRefGoogle Scholar
  11. Bird DM, Williamson VM, Abad P, McCarter J, Danchin EG, Castagnone-Sereno P, Opperman CH (2009) The genomes of root-knot nematodes. Annu Rev Phytopathol 47:333–351PubMedCrossRefGoogle Scholar
  12. Boisson-Dernier A, Andriankaja A, Chabaud M, Niebel A, Journet EP, Barker DG, de Carvalho-Niebel F (2005) MtENOD11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence. Mol Plant Microbe Interact 18:1269–1276PubMedCrossRefGoogle Scholar
  13. Caillaud MC, Abad P, Favery B (2008a) Cytoskeleton reorganization: a key process in root-knot nematode-induced giant cell ontogenesis. Plant Signal Behav 3:816–818PubMedCentralPubMedCrossRefGoogle Scholar
  14. Caillaud MC, Dubreuil G, Quentin M, Perfus-Barbeoch L, Lecomte P, de Almeida Engler J, Abad P, Rosso MN, Favery B (2008b) Root-knot nematodes manipulate plant cell functions during a compatible interaction. J Plant Physiol 165:104–113PubMedCrossRefGoogle Scholar
  15. Caillaud MC, Lecomte P, Jammes F, Quentin M, Pagnotta S, Andrio E, de Almeida Engler J, Marfaing N, Gounon P, Abad P, Favery B (2008c) MAP65-3 microtubule-associated protein is essential for nematode-induced giant cell ontogenesis in Arabidopsis. Plant Cell 20:423–437PubMedCentralPubMedCrossRefGoogle Scholar
  16. Cebolla A, Vinardell JM, Kiss E, Olah B, Roudier F, Kondorosi A, Kondorosi E (1999) The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J 18:4476–4484PubMedCrossRefGoogle Scholar
  17. Clement M, 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 of Arabidopsis. Plant Cell 21:2963–2979PubMedCentralPubMedCrossRefGoogle Scholar
  18. Cramer CL, Weissenborn DL, Cotttingham CK, Denbow CJ, Eisenbach JD, Radin DN, Yu X (1993) Regulation of defense-related gene expression during plant-pathogen interactions. J Nematol 25:507–551PubMedCentralPubMedGoogle Scholar
  19. Crespi M, Frugier F (2008) De novo organ formation from differentiated cells: root nodule organogenesis. Sci Signal 1:re11PubMedCrossRefGoogle Scholar
  20. Danchin EG, Rosso MN, Vieira P, de Almeida-Engler J, Coutinho PM, Henrissat B, Abad P (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci USA 107:17651–17656PubMedCrossRefGoogle Scholar
  21. Das S, DeMason DA, Ehlers JD, Close TJ, Roberts PA (2008) Histological characterization of root-knot nematode resistance in cowpea and its relation to reactive oxygen species modulation. J Exp Bot 59:1305–1313PubMedCrossRefGoogle Scholar
  22. Davis EL, Hussey RS, Baum TJ (2004) Getting to the roots of parasitism by nematodes. Trends Parasitol 20:134–141PubMedCrossRefGoogle Scholar
  23. de Almeida Engler J, De Vleesschauwer V, Burssens S, Celenza JL Jr, Inze 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 11:793–808PubMedCentralPubMedGoogle Scholar
  24. de Almeida Engler J, Van Poucke K, Karimi M, De Groodt R, Gheysen G, Engler G (2004) Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. Plant J 38:12–26PubMedCrossRefGoogle Scholar
  25. de Almeida Engler J, Rodiuc N, Smertenko A, Abad P (2010) Plant actin cytoskeleton re-modelling by plant parasitic nematodes. Plant Signal Behav 5:1–5CrossRefGoogle Scholar
  26. del Giudice J, Cam Y, Damiani I, Fung-Chat F, Meilhoc E, Bruand C, Brouquisse R, Puppo A, Boscari A (2011) Nitric oxide is required for an optimal establishment of the Medicago truncatulaSinorhizobium meliloti symbiosis. New Phytol 191:405–417Google Scholar
  27. Ehsanpour AA, Jones MGK (1996) Glucuronidase expression in transgenic tobacco roots with a Parasponia promoter on infection with Meloidogyne javanica. J Nematol 28:407–413PubMedCentralPubMedGoogle Scholar
  28. Escobar C, De Meutter J, Aristizabal FA, Sanz-Alferez S, del Campo FF, Barthels N, Van der Eycken W, Seurinck J, van Montagu M, Gheysen G, Fenoll C (1999) Isolation of the LEMMI9 gene and promoter analysis during a compatible plant-nematode interaction. Mol Plant Microbe Interact 12:440–449PubMedCrossRefGoogle Scholar
  29. Escobar C, Barcala M, Portillo M, Almoguera C, Jordano J, Fenoll C (2003) Induction of the Hahsp17.7G4 promoter by root-knot nematodes: involvement of heat-shock elements in promoter activity in giant cells. Mol Plant Microbe Interact 16:1062–1068PubMedCrossRefGoogle Scholar
  30. Favery B, Lecomte P, Gil N, Bechtold N, Bouchez D, Dalmasso A, Abad P (1998) RPE, a plant gene involved in early developmental steps of nematode feeding cells. EMBO J 17:6799–6811PubMedCrossRefGoogle Scholar
  31. 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
  32. Favery B, Chelysheva LA, Lebris M, Jammes F, Marmagne A, De Almeida-Engler J, Lecomte P, Vaury C, Arkowitz RA, Abad P (2004) Arabidopsis formin AtFH6 is a plasma membrane-associated protein upregulated in giant cells induced by parasitic nematodes. Plant Cell 16:2529–2540PubMedCentralPubMedCrossRefGoogle Scholar
  33. Frendo P, Harrison J, Norman C, Hernandez Jimenez MJ, Van de Sype G, Gilabert A, Puppo A (2005) Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Mol Plant Microbe Interact 18:254–259PubMedCrossRefGoogle Scholar
  34. Fuller VL, Lilley CJ, Atkinson HJ, Urwin P (2007) Differential gene expression in Arabidopsis following infection by plant-parasitic nematodes Meloidogyne incognita and Heterodera schachtii. Mol Plant Pathol 8:595–609PubMedCrossRefGoogle Scholar
  35. Gal TZ, Aussenberg ER, Burdman S, Kapulnik Y, Koltai H (2006) Expression of a plant expansin is involved in the establishment of root knot nematode parasitism in tomato. Planta 224:155–162PubMedCrossRefGoogle Scholar
  36. Gao X, Starr J, Gobel C, Engelberth J, Feussner I, Tumlinson J, Kolomiets M (2008) Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defense genes, and resistance to root-knot nematodes. Mol Plant Microbe Interact 21:98–109PubMedCrossRefGoogle Scholar
  37. Gheysen G, Fenoll C (2002) Gene expression in nematode feeding sites. Annu Rev Phytopathol 40:191–219PubMedCrossRefGoogle Scholar
  38. Gheysen G, Van der Eychen W, Barthels N, Karimi M, Van Montagu M (1996) The exploitation of nematode-responsive plant genes in novel nematode control methods. Pesticide Sci 47:95–101CrossRefGoogle Scholar
  39. Goddijn OJM, Lindsey K, Van der Lee FM, Klap JC, Sijmons PC (1993) Differential gene expression in nematode-induced feeding structures of transgenic plants harbouring promoter-gusA fusion constructs. Plant J 4:863–873PubMedCrossRefGoogle Scholar
  40. Goellner M, Wang X, Davis EL (2001) Endo-beta-1,4-glucanase expression in compatible plant-nematode interactions. Plant Cell 13:2241–2255PubMedCentralPubMedGoogle Scholar
  41. 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
  42. Grunewald W, Karimi M, Wieczorek K, Van de Cappelle E, Wischnitzki E, Grundler F, Inze D, Beeckman T, Gheysen G (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148:358–368PubMedCentralPubMedCrossRefGoogle Scholar
  43. Grunewald W, Cannoot B, Friml J, Gheysen G (2009a) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog 5:e1000266PubMedCentralPubMedCrossRefGoogle Scholar
  44. 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 21:2553–2562PubMedCentralPubMedCrossRefGoogle Scholar
  45. Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant Microbe Interact 22:763–772PubMedCrossRefGoogle Scholar
  46. Hamamouch N, Li C, Seo PJ, Park C-M, Davis EL (2010) Expression of Arabidopsis pathogenesis-related genes during nematode infection. Mol Plant Pathol 12:355–364Google Scholar
  47. 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
  48. Hammes UZ, Nielsen E, Honaas LA, Taylor CG, Schachtman DP (2006) AtCAT6, a sink-tissue-localized transporter for essential amino acids in Arabidopsis. Plant J 48:414–426PubMedCrossRefGoogle Scholar
  49. Hansen E, Harper G, McPherson MJ, Atkinson HJ (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 48:161–170CrossRefGoogle Scholar
  50. Harrison MJ (1999) Biotrophic interfaces and nutrient transport in plant/fungal symbioses. J Exp Bot 50:1013–1022CrossRefGoogle Scholar
  51. Huang X, Springer PS, Kaloshian I (2003) Expression of the Arabidopsis MCM Gene PROLIFERA during root-knot and cyst nematode infection. Phytopathology 93:35–41PubMedCrossRefGoogle Scholar
  52. Huang G, Dong R, Allen R, Davis EL, Baum TJ, Hussey RS (2006) A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol Plant Microbe Interact 19:463–470PubMedCrossRefGoogle Scholar
  53. Huo X, Schnabel E, Hughes K, Frugoli J (2006) RNAi Phenotypes and the localization of a protein::GUS fusion imply a role for Medicago truncatula PIN genes in nodulation. J Plant Growth Regul 25:156–165PubMedCentralPubMedCrossRefGoogle Scholar
  54. 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
  55. Jammes F, Lecomte P, de 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
  56. Jones MGK, Payne HL (1978) Early stages of nematode-induced giant cell formation in roots of Impatiens balsamina. J Nematol 10:70–84PubMedCentralPubMedGoogle Scholar
  57. 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
  58. Karczmarek A, Fudali S, Lichocka M, Sobczak M, Kurek W, Janakowski S, Roosien J, Golinowski W, Bakker J, Goverse A, Helder J (2008) Expression of two functionally distinct plant endo-beta-1,4-glucanases is essential for the compatible interaction between potato cyst nematode and its hosts. Mol Plant Microbe Interact 21:791–798PubMedCrossRefGoogle Scholar
  59. Karimi M, de Oliveira Manes C-L, Van Montagu M, Gheysen G (2002) Activation of a Pgrp-gus fusion in Arabidopsis thaliana roots upon nematode infection. J Nematol 34:75–79PubMedCentralPubMedGoogle Scholar
  60. 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
  61. Lilley CJ, Urwin PE, Johnston KA, Atkinson HJ (2004) Preferential expression of a plant cystatin at nematode feeding sites confers resistance to Meloidogyne incognita and Globodera pallida. Plant Biotechnol J 2:3–12PubMedCrossRefGoogle Scholar
  62. Lipka V, Panstruga R (2005) Dynamic cellular responses in plant-microbe interactions. Curr Opin Plant Biol 8:625–631PubMedCrossRefGoogle Scholar
  63. Lohar DP, Bird DM (2003) Lotus japonicus: a new model to study root-parasitic nematodes. Plant Cell Physiol 44:1176–1184PubMedCrossRefGoogle Scholar
  64. 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
  65. Mathesius U, Schlaman HR, Spaink HP, Of Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14:23–34PubMedCrossRefGoogle Scholar
  66. Maunoury N, Redondo-Nieto M, Bourcy M, Van de Velde W, Alunni B, Laporte P, Durand P, Agier N, Marisa L, Vaubert D, Delacroix H, Duc G, Ratet P, Aggerbeck L, Kondorosi E, Mergaert P (2010) Differentiation of symbiotic cells and endosymbionts in Medicago truncatula nodulation are coupled to two transcriptome-switches. PLoS One 5:e9519PubMedCentralPubMedCrossRefGoogle Scholar
  67. 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
  68. 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
  69. Mitchum MG, Sukno S, Wang X, Shani Z, Tsabary G, Shoseyov O, Davis EL (2004) The promoter of the Arabidopsis thaliana Cel1 endo-1,4-ß glucanase gene is differentially expressed in plant feeding cells induced by root-knot and cyst nematodes. Mol Plant Pathol 5:175–181PubMedCrossRefGoogle Scholar
  70. Møller SG, Urwin PE, Atkinson HJ, Mc-Pherson MJ (1998) Nematode-induced expression of atao1, a gene encoding an extracellular diamine oxidase associated with developing vascular tissue. Physiol Mol Plant Pathol 53:73–79CrossRefGoogle Scholar
  71. Niebel A, De Almeida Engler J, Tire C, Engler G, Van Montagu M, Gheysen G (1993) Induction patterns of an extensin gene in tobacco upon nematode infection. Plant Cell 5:1697–1710PubMedCentralPubMedGoogle Scholar
  72. Niebel A, de Almeida Engler J, Hemerly A, Ferreira P, Inze D, Van Montagu M, Gheysen G (1996) Induction of cdc2a and cyc1At expression in Arabidopsis thaliana during early phases of nematode-induced feeding cell formation. Plant J 10:1037–1043PubMedCrossRefGoogle Scholar
  73. Opperman CH, Taylor CG, Conkling MA (1994) Root-knot nematode-directed expression of a plant root-specific gene. Science 263:221–223PubMedCrossRefGoogle Scholar
  74. Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 3:320–328PubMedCrossRefGoogle Scholar
  75. Patriarca EJ, Tate R, Ferraioli S, Iaccarino M (2004) Organogenesis of legume root nodules. Int Rev Cytol 234:201–262PubMedCrossRefGoogle Scholar
  76. Pauly N, Pucciariello C, Mandon K, Innocenti G, Jamet A, Baudouin E, Herouart D, Frendo P, Puppo A (2006) Reactive oxygen and nitrogen species and glutathione: key players in the legume-Rhizobium symbiosis. J Exp Bot 57:1769–1776PubMedCrossRefGoogle Scholar
  77. Quentin M, Allasia V, Pegard A, Allais F, Ducrot PH, Favery B, Levis C, Martinet S, Masur C, Ponchet M, Roby D, Schlaich NL, Jouanin L, Keller H (2009) Imbalanced lignin biosynthesis promotes the sexual reproduction of homothallic oomycete pathogens. PLoS Pathog 5:e1000264PubMedCentralPubMedCrossRefGoogle Scholar
  78. Richardson L, Price NS (1984) Observations on the biology of Meloidogyne incognita and the diageotropica tomato mutant. Rev Nématol 7:97–99Google Scholar
  79. Santos R, Herouart D, Sigaud S, Touati D, Puppo A (2001) Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol Plant Microbe Interact 14:86–89PubMedCrossRefGoogle Scholar
  80. Schmidt SM, Panstruga R (2007) Cytoskeleton functions in plant-microbe interactions. Physiol Mol Plant Pathol 71:135–148CrossRefGoogle Scholar
  81. Scholl EH, Thorne JL, McCarter JP, Bird DM (2003) Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. Genome Biol 4:R39PubMedCentralPubMedCrossRefGoogle Scholar
  82. Strittmatter G, Gheysen G, Gianinazzi-Pearson V, Hahn K, Niebel A, Rohde W, Tacke E (1996) Infections with various types of organisms stimulate transcription from a short promoter fragment of the potato gst1 gene. Mol Plant Microbe Interact 9:68–73PubMedCrossRefGoogle Scholar
  83. Takemoto D, Hardham AR (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136:3864–3876PubMedCentralPubMedCrossRefGoogle Scholar
  84. Trudgill DL, Blok VC (2001) Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu Rev Phytopathol 39:53–77PubMedCrossRefGoogle Scholar
  85. Van de Cappelle E, Plovie E, Kyndt T, Grunewald W, Cannoot B, Gheysen G (2008) AtCDKA;1 silencing in Arabidopsis thaliana reduces reproduction of sedentary plant-parasitic nematodes. Plant Biotechnol J 6:749–757PubMedCrossRefGoogle Scholar
  86. van Noorden GE, Kerim T, Goffard N, Wiblin R, Pellerone FI, Rolfe BG, Mathesius U (2007) Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol 144:1115–1131PubMedCentralPubMedCrossRefGoogle Scholar
  87. Vanholme B, De Meutter J, Tytgat T, Van Montagu M, Coomans A, Gheysen G (2004) Secretions of plant-parasitic nematodes: a molecular update. Gene 332:13–27PubMedCrossRefGoogle Scholar
  88. Vercauteren I, Goeleven E, Barthels N, Van Montagu M, Gheysen G (1998) The rha1 gene, encoding a small GTP binding protein, is induced in nematode infection sites. Arch Physiol Biochem 106:158 (B130)Google Scholar
  89. Vercauteren I, Van Der Schueren E, Van Montagu M, Gheysen G (2001) Arabidopsis thaliana genes expressed in the early compatible interaction with root-knot nematodes. Mol Plant Microbe Interact 14:288–299PubMedCrossRefGoogle Scholar
  90. Vercauteren I, de Almeida Engler J, De Groodt R, Gheysen G (2002) An Arabidopsis thaliana pectin acetylesterase gene is upregulated in nematode feeding sites induced by root-knot and cyst nematodes. Mol Plant Microbe Interact 15:404–407PubMedCrossRefGoogle Scholar
  91. Vinardell JM, Fedorova E, Cebolla A, Kevei Z, Horvath 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 15:2093–2105PubMedCentralPubMedCrossRefGoogle Scholar
  92. Wang Z, Potter RH, Jones MGK (2003) Differential display analysis of gene expression in the cytoplasm of giant cells induced in tomato roots by Meloidogyne javanica. Mol Plant Pathol 4:361–371PubMedCrossRefGoogle Scholar
  93. Wang X, Replogle A, Davis E, Mitchum M (2007) The tobacco Cel7 gene promoter is auxin-responsive and locally induced in nematode feeding sites of heterologous plants. Mol Plant Pathol 8:423–436PubMedCrossRefGoogle Scholar
  94. Wasson AP, Ramsay K, Jones MG, Mathesius U (2009) Differing requirements for flavonoids during the formation of lateral roots, nodules and root knot nematode galls in Medicago truncatula. New Phytol 183:167–179PubMedCrossRefGoogle Scholar
  95. Weerasinghe RR, Bird DM, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proc Natl Acad Sci USA 102:3147–3152PubMedCrossRefGoogle Scholar
  96. Wiggers RJ, Thornton NT, Starr JL (2002) The effects of colchicine on number of giant cell nuclei and nematode development in Pisum sativum infected by Meloidogyne incognita. Nematology 4:107–109CrossRefGoogle Scholar
  97. Wildermuth MC (2010) Modulation of host nuclear ploidy: a common plant biotroph mechanism. Curr Opin Plant Biol 13:449–458PubMedCrossRefGoogle Scholar
  98. Wuyts N, Lognay G, Swennen R, De Waele D (2006) Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. J Exp Bot 57:2825–2835PubMedCrossRefGoogle Scholar
  99. Yokota K, Fukai E, Madsen LH, Jurkiewicz A, Rueda P, Radutoiu S, Held M, Hossain MS, Szczyglowski K, Morieri G, Oldroyd GE, Downie JA, Nielsen MW, Rusek AM, Sato S, Tabata S, James EK, Oyaizu H, Sandal N, Stougaard J (2009) Rearrangement of actin cytoskeleton mediates invasion of Lotus japonicus roots by Mesorhizobium loti. Plant Cell 21:267–284PubMedCentralPubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Bruno Favery
    • 1
    • 2
    • 3
  • Michaël Quentin
    • 1
    • 2
    • 3
  • Pierre Abad
    • 1
    • 2
    • 3
    Email author
  1. 1.Interactions Biotiques et Santé Végétale, INRA, UMR 1301Sophia AntipolisFrance
  2. 2.Interactions Biotiques et Santé Végétale, CNRS, UMR 6243Sophia AntipolisFrance
  3. 3.Interactions Biotiques et Santé Végétale, INRA-CNRS-Université de Nice Sophia-Antipolis, UMR 1301-6243Sophia AntipolisFrance

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