The Role of Plant Hormones in Nematode Feeding Cell Formation

  • Aska Goverse
  • David Bird


In this Chapter, we discuss recent advances in the role of plant hormones in the molecular mechanisms underlying feeding cell formation both by cyst (CN) and root-knot nematodes (RKN). Phytohormones are small signalling molecules that regulate plant growth and development, including the formation of highly specialized root structures like nematode feeding cells. High-throughput transcriptome profiling has facilitated the identification of an increasing number of novel hormone related genes that are differentially expressed during feeding cell development. Together with dedicated functional studies, a picture has emerged which points to plant hormones playing an important role in the reprogramming of gene expression patterns upon nematode infection. Here, we present a comprehensive overview of the role of classical plant hormones, including cytokinin, auxin and ethylene, in the establishment of nematode-induced regulatory networks upon infection of plant roots. We also discuss the role of small peptides as a novel class in plant hormone signalling during feeding cell formation.


Auxin Transport Cyst Nematode Nematode Infection Polar Auxin Transport Cytokinin Response 
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.


  1. Abad P, Gouzy, J, Aury JM, Castagnone-Sereno P, Danchin EG, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC, Caillaud MC, Coutinho PM, Dasilva C, De Luca F, DeauF, Esquibet M, Flutre T, Goldstone JV, Hamamouch N, Hewezi T, Jaillon O, Jubin C, Leonetti P, Magliano M, Maier TR, Markov GV, McVeigh P, Pesole G, Poulain J, Robinson-Rechavi M, Sallet E, Ségurens B, Steinbach D, Tytgat T, Ugarte E, van Ghelder C, Veronico P, Baum TJ, Blaxter M, Bleve-Zacheo T, Davis EL, Ewbank JJ, Favery B, Grenier E, Henrissat B, Jones JT, Laudet V, Maule AG, Quesneville H, Rosso MN, Schiex T, Smant G, Weissenbach J, Wincker P (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotech 26:909–915CrossRefGoogle Scholar
  2. Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17PubMedCrossRefGoogle Scholar
  3. Abeles FB, Morgan PW, Saltveit ME Jr (1992) Ethylene in plant biology, 2nd edn. Academic Press, NewYorkGoogle Scholar
  4. Abel S, Nguyen MD, Chow W, Theologis A (1995) ACS4, a primary indole-acitic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. J Biol Chem 27:19093–19099Google Scholar
  5. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284:2148–2152PubMedCrossRefGoogle Scholar
  6. Balasubramaniam M, Rangaswami G (1962) Presence of indole compounds in nematode galls. Nature 194:714–715CrossRefGoogle Scholar
  7. Bers NEM van (2008) Characterization of genes coding for small hypervariable peptides in Globodera rostochiensis. PhD thesis. Wageningen, The NetherlandsGoogle Scholar
  8. Bird AF (1975) Symbiotic relationships between nematodes and plants. Symp Soc Exp Bio 29:351–371Google Scholar
  9. Bird AF, Loveys BR (1980) The involvement of cytokinins in a host-parasite relationship between the tomato (Lycopersicon esculentum) and a nematode (Meloidogyne javanica). Parasitology 80:497–505CrossRefGoogle Scholar
  10. Bird DMcK (1996) Manipulation of host gene expression by root-knot nematodes. J Parasitol 82:881–888PubMedCrossRefGoogle Scholar
  11. Bird DMcK (2004) Signaling between nematodes and plants. Curr Opin Plant Biol 7:372–376PubMedCrossRefGoogle Scholar
  12. Butenko MA, Vie AK, Brembu T, Aalen RB, Bones AM (2009) Plant peptides in signalling: looking for new partners. Trends Plant Sci 14:255–263PubMedCrossRefGoogle Scholar
  13. Buzasa DM, Gresshoff PM (2007) Short- and long-distance control of root development by LjHAR1 during the juvenile stage of Lotus japonicus. J Plant Physiol 164:52–459CrossRefGoogle Scholar
  14. Carles CC, Fletcher JC (2003) Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci 8:394–401PubMedCrossRefGoogle Scholar
  15. Chae HS, Faure F, Kieber JJ (2003) The eto1,eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS proteins. Plant Cell 15:545–559PubMedCrossRefGoogle Scholar
  16. Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–545PubMedCrossRefGoogle Scholar
  17. Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Ann Rev Genet 43:265–285PubMedCrossRefGoogle Scholar
  18. Clark SE (2001) Cell signalling at the shoot meristem. Nat Rev 2:276–284CrossRefGoogle Scholar
  19. Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM (1996) The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122:1567–1575PubMedGoogle Scholar
  20. D’Agostino IB, Kieber JJ (1999) Phosphorelay signal transduction: the emerging family of plant response regulators. Trends Biochem Sci 24:452–456PubMedCrossRefGoogle Scholar
  21. Davies PJ (1995) The plant hormones: their nature, occurrence and functions. In: Davies PJ (ed) Plant hormones: physiology, biochemistry and molecular biology. Kluwer Academic, The Netherlands, pp. 1–12Google Scholar
  22. Davis EL, Hussey RS, Mitchum MG, Baum TJ (2008) Parasitism proteins in nematode-plant interactions. Curr Opin Plant Biol 11:360–366PubMedCrossRefGoogle Scholar
  23. De Almeida Engler J, Vleesschauwer VD, Burssens S, Celenza JL Jr, 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 11:793–807PubMedGoogle Scholar
  24. de Meutter J, Tytgat T, Witters E, Gheysen G, van Onckelen H, Gheysen G (2003) Identification of cytokinins produced by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Mol Plant Pathol 4:271–277PubMedCrossRefGoogle Scholar
  25. de Meutter J, Tytgat T, Prinsen E, Gheysen G, van Onckelen H, Gheysen G (2005) Production of auxin and related compounds by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Commun Agric Appl Biol Sci 70:51–60PubMedGoogle Scholar
  26. Dintilhac A, Bernués J (2002) HMGB1 interacts with many apparently unrelated proteins by recognizing short amino acid sequences. J Biol Chem 277:7021–7028PubMedCrossRefGoogle Scholar
  27. Dropkin VH (1969) The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology 59:1632–1637Google Scholar
  28. Dropkin VH, Helgeson JP, Upper CD (1969) The hypersensitivity reaction of tomato resistant to Meloidogyne incognita: Reversal by cytokinins. J Nematol 1:55–61PubMedGoogle Scholar
  29. Dun EA, Brewer PB, Beveridge CA (2009) Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci 14:364–372PubMedCrossRefGoogle Scholar
  30. Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu CM (2005) The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell 17:2542–2553PubMedCrossRefGoogle Scholar
  31. Francis D, Sorrel DA (2001) The interface between the cell cycle and plant growth regulators: a mini review. J Plant Growth Regul 33:1–12CrossRefGoogle Scholar
  32. Friml J (2010) Subcellular trafficking of PIN auxin efflux carriers in auxin transport. Eur J Cell Biology 89:231–235CrossRefGoogle Scholar
  33. Fuller VL, Lilley CJ, Atkinson HJ, Urwin PE (2007) Differential expression in Arabidopsis following infection by plant-parasitic nematodes Meloidogyne incognita and Heterodera schachtii. Mol Plant Pathol 8:595–609PubMedCrossRefGoogle Scholar
  34. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2001) Identification of putative parasitsm genes expressed in the esophageal glands of the soybean cyst nematode, Heterodera glycines. Mol Plant Microbe Interact 14:1247–1254PubMedCrossRefGoogle Scholar
  35. Gheysen G, Mitchum MG (2009) Molecular insights in the susceptible plant response to nematode infection. In: Berg RH, Taylor CG (eds) Cell biology of plant nematode parasitism. Plant cell Monographs. Springer, New York, p 45CrossRefGoogle Scholar
  36. 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
  37. Glazer I, Apelbaum A, Orion D (1985) Effect of inhibitors and stimulators of ethylene production on gall development in Meloidogyne javanica-infected tomato roots. J Nematol 17:145–149PubMedGoogle Scholar
  38. Goodey JB (1948) The galls caused by Anguillulina balsamophila (Thorne) Goodey on the leaves of Wyethia amplexicaulis Nutt and Balsamorhiza sagittata. J Helminthol 22:109–116PubMedCrossRefGoogle Scholar
  39. Goverse A, Rouppe van der Voort J, Roupe van der Voort C, Kavelaars A, Smant G, Schots A, Bakker J, Helder J (1999) Naturally-induced secretions of the potato cyst nematode co-stimulate the proliferation of both tobacco leaf protoplasts and human peripheral blood mononuclear cells. Mol Plant Microbe Interact 12:872–881PubMedCrossRefGoogle Scholar
  40. Goverse A, de Almeida Engler J, Verhees J, Krol van der S, Helder J, Gheysen G (2000a) Cell cycle activation by plant-parasitic nematodes. Plant Mol Biol 43:747–761CrossRefGoogle Scholar
  41. Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder J (2000b) Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Mol Plant Microbe Interact 13:1121–1129CrossRefGoogle Scholar
  42. Grun S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57:507–516PubMedCrossRefGoogle Scholar
  43. Grunewald W, Karimi M, Wieczorek K, Van de Capelle E, Grundler F, Beeckman T, Inze D, Gheysen G (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148:358–368PubMedCrossRefGoogle Scholar
  44. Grunewald W, Cannoot B, Friml J, Gheysen G (2009a) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLOS Pathogens 5:e1000266CrossRefGoogle Scholar
  45. Grunewald W, Van Noorden G, Van Listerdael G, Beeckman T, Gheysen G (2009b) Manipulation of auxin transport in plant roots during rhizobium symbiosis and nematode parasitism. Plant Cell 21:2553–2562CrossRefGoogle Scholar
  46. Guilfoyle TJ, Ulmasov T, Hagen G (1998) The ARF family of transcription factors and their role in plant hormone-responsive transcription. Cell Mol Life Sci 54:619–627PubMedCrossRefGoogle Scholar
  47. Hermsmeier D, Mazarei M, Baum TJ (1998) Differential display analysis of the compatible interacttion between soybean and the soybean cyst nematode. Mol Plant Microbe Interact 11:1258–1263CrossRefGoogle Scholar
  48. 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
  49. Hirano K, Ueguchi-Tanaka M, Matska M (2008) GID1-mediated gibberellin signalling in plants. Trends Plant Sci 13:192–199PubMedCrossRefGoogle Scholar
  50. Hirayama T, Shimozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351PubMedCrossRefGoogle Scholar
  51. Hirsch S, Kim J, Muñoz A, Heckmann AB, Downie JA, Oldroyd GE (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21:545–557PubMedCrossRefGoogle Scholar
  52. Hobe M, Müller R, Grünewald M, Brand U, Simon R (2003) Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol 213:371–381PubMedCrossRefGoogle Scholar
  53. Huang G, Gao B, Maier T, Allen R, Davis EL, Baum TJ, Hussey RS (2003) A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol Plant Microbe Interact 16:376–381PubMedCrossRefGoogle Scholar
  54. 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
  55. Hutangura P, Matthesius 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
  56. Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG (2007a) Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol Plant Microbe Interact 20:10–25Google Scholar
  57. Ithal N, Recknor J, Nettleton D, Hearne L, Maier T, Baum TJ, Mitchum MG (2007b) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol Plant Microbe Interact 20:293–305CrossRefGoogle Scholar
  58. Jammes F, Lecomte TN, 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 4:447–458CrossRefGoogle Scholar
  59. Jones MGK (1981) Host cell responses to endoparasitic nematode attack: structure and function of giant-cells and syncytia. Ann Appl Biol 97:353–372CrossRefGoogle Scholar
  60. Jones JT, Furlanetto C, Bakker E, Banks B, Blok V, Chen Q, Phillips MS, Prior A (2003) Characterization of a chorismate mutase from the potato cyst nematode Globodera pallida. Mol Plant Pathol 4:43–50PubMedCrossRefGoogle Scholar
  61. Jones JT, Furlanetto C, Phillips MS (2007) The role of flavonoids produced in response to cyst nematode infection of Arabidopsis thaliana. Nematology 9:671–677CrossRefGoogle Scholar
  62. 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 Pathology 5:343–346CrossRefGoogle Scholar
  63. Karczmarek A, Fudali S, Lichocka M, Sobzcak M, Kurek W, Janakoski 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
  64. Kinoshita A, Nakamura Y, Sasaki E, Kyozuka J, Fukuda H, Sawa S (2007) Gain-of-Function Phenotypes of Chemically Synthetic CLAVATA3/ESR-Related (CLE) Peptides in Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol 48:1821–1825.PubMedCrossRefGoogle Scholar
  65. Koltai H, Dhandaydham M, Opperman C, Tomas 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
  66. Krupasagar V, Barker KR (1969) Increased cytokinin concentrations in tobacco infected with the root-knot nematode Meloidogyne incognita. Phytopathology 56:885Google Scholar
  67. Li Y, Fester T, Taylor C (2009) Transcriptomic analysis of nematode infestation. In: Berg RH, Taylor CG (eds) Cell biology of plant nematode parasitism. Plant cell Monographs.Springer, New York, p 189CrossRefGoogle Scholar
  68. Lin Z, Zhong S, Grierson D (2009) Recent advances in ethylene research. J Exp Bot 60:3311–3336PubMedCrossRefGoogle Scholar
  69. Loake G, Grant M (2007) Salicylic acid in plant defence-the players and protagonists. Curr Opin Plant Biol 10:466–472PubMedCrossRefGoogle Scholar
  70. Lohar DP, Bird DMcK (2003) Lotus japonicus: A new model to study root-parasitic nematodes. Plant Cell Physiol 44:1176–1184PubMedCrossRefGoogle Scholar
  71. Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DMcK (2004) Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. Plant J 38:203–214PubMedCrossRefGoogle Scholar
  72. 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
  73. Mathesius U (2003) Conservation and divergence of signalling pathways between roots and soil microbes—the Rhizobium-legume symbiosis compared to the development of lateral roots, mycorrhizal interactions and nematode-induced galls. Plant Soil 255:105–119CrossRefGoogle Scholar
  74. 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
  75. Mazarei M, Elling AA, Maier TR, Puthoff DP, Baum TJ (2007) GmEREBP1 is a transcription factor activating defense genes in soybean and Arabidopsis. Mol Plant Microbe Interact 20:107–119PubMedCrossRefGoogle Scholar
  76. McGurl B, Pearce G, Orozco-Cardenas M, Ryan CA (1992) Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255:1570–1573PubMedCrossRefGoogle Scholar
  77. Mitchum MG, Wang X-H, Davis EL (2008) Diverse and conserved roles of CLE peptides. Curr Opin Plant Biol 11:75–81PubMedCrossRefGoogle Scholar
  78. Oh K, Ivanchenko MG, White TJ, Lomax TL (2006) The diageotropica gene of tomato encodes a cyclophilin: a novel player in auxin signalling. Planta 224:133–144PubMedCrossRefGoogle Scholar
  79. Ohyama K et al (2008) Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J 55:152–160PubMedCrossRefGoogle Scholar
  80. Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50:67–77PubMedCrossRefGoogle Scholar
  81. Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Ann Rev Plant Biol 59:519–546CrossRefGoogle Scholar
  82. Olsen AN, Skriver K (2003) Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3. Trends Plant Sci 8:55–57PubMedCrossRefGoogle Scholar
  83. Opperman CH, Bird DMcK, Williamson VM, Rohksar DS, Burke M, Cohn J, Cromer J, Diener S, Gajan J, Graham S, Houfek TD, Liu Q-L, Mitros T, Schaff JE, Schaffer R, Scholl E, Sosinski BR, Thomas VP, Windham E (2008) Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism. Proc Natl Acad Sci USA 105:14802–14807PubMedCrossRefGoogle Scholar
  84. Puthoff PD, Ehrenfeld ML, Vinyard BT, Tucker ML (2007) Genechip profiling of transcriptional responses to soybean cyst nematode Heterodera glycines colonization of soybean roots. J Exp Bot 58:3407–3418PubMedCrossRefGoogle Scholar
  85. Redig P, Shaul O, Inzé D, van Montagu M and, Onckelen H (1996) Levels of endogenous cytokinins, indole-3-acetic acid and abscisic acid during cell cycle of synchronized tobacco BY-2 cells. FEBS Letts 391:175–180CrossRefGoogle Scholar
  86. Richardson L, Price NS (1984) Observations on the biology of Meloidogyne incognita and the diageotropica tomato mutant. Rev Nematol 7:97–99Google Scholar
  87. Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078PubMedCrossRefGoogle Scholar
  88. Schmülling T (2002) New insights into the functions of cytokinins in plant development. J Plant Growth Reg 21:40–49CrossRefGoogle Scholar
  89. Schnabel E, Journet EP, de Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 58:809–822PubMedCrossRefGoogle Scholar
  90. Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signalling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE 3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12:3703–3714PubMedCrossRefGoogle Scholar
  91. Soto MJ, Fernandez-Aparicio M, Castellanos-Morales V, Garcia-Garrido JM, Ocampo JA, Delgado MJ, Vierheilig H (2010) First indications for the involvement of strigolactones on nodule formation in alfala (Medicago sativa). Soil Biol Biochem 42:383–385CrossRefGoogle Scholar
  92. Swiecicka M, Filipecki M, Lont D, Van Vliet J, Qin L, Goverse A, Bakker J, Helder J (2009) Dynamics in the tomato root transcriptome on infection with the potato cyst nematode Globodera rostochiensis. Mol Plant Pathol 10:487–500PubMedCrossRefGoogle Scholar
  93. Symons GM, Ross JJ, Jager CE, Reid JB (2008) Brassinosteroid transport. J Exp Bot 59:17–24PubMedCrossRefGoogle Scholar
  94. Tucker ML, Xue P, Yang R (2010) 1-Aminocyclopropane -1 carboxylic acid (ACC) concentration and ACC synthase expression in soybean roots, root tips, and soybean cyst nematode (Heterodera glycines)-infected roots. J Exp Bot 61:463–472PubMedCrossRefGoogle Scholar
  95. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971PubMedGoogle Scholar
  96. Viglierchio DR, Yu PK (1968) Plant parasitic nematodes: a new mechanism for injury of hosts. Science 147:1301–1303CrossRefGoogle Scholar
  97. Wang G, Fiers M (2009) CLE peptide signaling during plant development. Protoplasma 240:33–34PubMedCrossRefGoogle Scholar
  98. Wang KL, Yoshida H, Lurin C, Ecker JR (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428:945–950PubMedCrossRefGoogle Scholar
  99. Wang XH, Mitchum MG, Gao B, Li C, Diab H, Baum TJ, Hussey RS, Davis EL (2005) A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol Plant Pathol 6:187–191PubMedCrossRefGoogle Scholar
  100. Wang X, Replogle A, Davis EL, Mitchum MG (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
  101. Wasson AP, Ramsay K, Jones MGK, Matthesus U (2009) Differing requirements for flavonoids during the formation of lateral roots, nodules and root knot nematode galls in Medicago truncatula. New Phytologist 183:167–179PubMedCrossRefGoogle Scholar
  102. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697PubMedCrossRefGoogle Scholar
  103. Weerasinghe RR, Bird DM, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus root hair cells. Proc Natl Acad Sci USA 102:3147–152PubMedCrossRefGoogle Scholar
  104. Weijers D, Franke-van Dijk M, Vencken R-J, Quint A, Hooykaas P, Offringa R (2001) An Arabidopsis minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128:4289–4299PubMedGoogle Scholar
  105. Werner T, Schmulling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538PubMedCrossRefGoogle Scholar
  106. Westwood JH, Bouwmeester H (2009) Parasitic plants tap into the main stream. New Phytol 184:284–287PubMedCrossRefGoogle Scholar
  107. Whitford R, Fernandez A, De Groodt R, Ortega E, Hilson P (2008) Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc Natl Acad Sci USA 105:18625–18630PubMedCrossRefGoogle Scholar
  108. Wieczorek K, Hoffman J, Bloch A, Szakasits D, Bohlman H, Grundler FMW (2008) Arabidopsis endo-1,4-glucanases are involved in the formation of root syncytia induced by Heterodera schachtii. Plant J 53:336–351PubMedCrossRefGoogle Scholar
  109. 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
  110. Wubben MJE, Rodermel SR, Baum TJ (2004) Mutation of a UDP-glucose-4-epimerase alters nematode susceptibility and ethylene responses in Arabidopsis roots. Plant J 40:712–724PubMedCrossRefGoogle Scholar
  111. 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
  112. Yamaguchi S (2008) Gibberellin metabolism and its regulation. Ann Rev Plant Biol 59:225–251CrossRefGoogle Scholar
  113. Yamagami T, Tsuchisaka A, Yamada K, Haddon WF, Harden A, Theologis A (2003) Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J Biol Chem 278:49102–49112PubMedCrossRefGoogle Scholar
  114. Yoo SD, Cho Y, Sheen J (2009) Emerging connections in the ethylene signalling network. Trends Plant Sci 14:270–279PubMedCrossRefGoogle Scholar
  115. Yoshida H, Nagata M, Saito K, Wang KL, Ecker JR (2005) Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 1-aminocyclopropane-1-carboxylate synthases. BMC Plant Biol 5:14PubMedCrossRefGoogle Scholar
  116. Zhang K, Letham DS, John PCL (1996) Cytokinin controls the cell cycle at mitosis by stimulating the tyrosine dephosphorylation and activation of p34cdc2-like H1 histone kinase. Planta 200:2–12PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Laboratory of NematologyWageningen UniversityWageningenThe Netherlands
  2. 2.Plant Nematode Genomes GroupNC State UniversityRaleighUSA

Personalised recommendations