Functional roles of effectors of plant-parasitic nematodes

Gene

Volumn 492, Issue 1, 2012, Pages 19-31

  Haegeman, Annelies ^a   Mantelin, Sophie ^b   Jones, John T ^b   Gheysen, Godelieve ^a  

^a GHENT UNIVERSITY   (Belgium)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

CLE; Effector; Parasitism gene; Plant parasitic nematode; Secretions

Indexed keywords

PHYTOHORMONE; PROTEOME; TRANSCRIPTOME;

GENOME; HORIZONTAL GENE TRANSFER; HOST PARASITE INTERACTION; HOST RESISTANCE; NEMATODAL PLANT DISEASE; NONHUMAN; PARASITISM; PLANT CELL; PLANT DEVELOPMENT; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; HELMINTH PROTEINS; HOST-PARASITE INTERACTIONS; NEMATODA; PLANT GROWTH REGULATORS; PLANT IMMUNITY; PLANTS; SIGNAL TRANSDUCTION; UBIQUITINATION;

FUNGI; NEMATODA;

EID: 84155195072     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2011.10.040     Document Type: Review

References (189)

1. Abad P., et al. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat. Biotechnol. 2008, 26:909-915.
2. Adam M.A.M., Phillips M.S., Jones J.T., Blok V.C. Characterisation of the cellulose-binding protein Mj-cbp-1 of the root knot nematode, Meloidogyne javanica. Physiol. Mol. Plant Pathol. 2008, 72:21-28.
3. Alcázar R., et al. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 2010, 231:1237-1249.
4. Bakhetia M., Urwin P.E., Atkinson H.J. qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Mol. Plant Microbe Interact. 2007, 20:306-312.
5. Bakhetia M., Urwin P.E., Atkinson H.J. Characterisation by RNAi of pioneer genes expressed in the dorsal pharyngeal gland cell of Heterodera glycines and the effects of combinatorial RNAi. Int. J. Parasitol. 2008, 38:1589-1597.
6. Bellafiore S., Shen Z.X., Rosso M.N., Abad P., Shih P., Briggs S.P. Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathog. 2008, 4:e1000192.
7. Benkova E., et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 2003, 115:591-602.
8. Bera-Maillet C., Arthaud L., Abad P., Rosso M.N. Biochemical characterization of MI-ENG1, a family 5 endoglucanase secreted by the root-knot nematode Meloidogyne incognita. Eur. J. Biochem. 2000, 267:3255-3263.
9. Birch P.R.J., et al. Towards understanding the virulence functions of RXLR effectors of the oomycete plant pathogen Phytophthora infestans. J. Exp. Bot. 2009, 60:1133-1140.
10. Bird D.M. Manipulation of host gene expression by root-knot nematodes. J. Parasitol. 1996, 82:881-888.
11. Bos J.I.B., Prince D., Pitino M., Maffei M.E., Win J., Hogenhout S.A. A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet. 2010, 6:e1001216.
12. Campbell A.M., Teesdale-Spittle P.H., Barrett J., Liebau E., Jefferies J.R., Brophy P.M. A common class of nematode glutathione S-transferase (GST) revealed by the theoretical proteome of the model organism Caenorhabditis elegans. Comp. Biochem. Physiol. B 2001, 128:701-708.
13. Castagnone-Sereno P., Wajnberg E., Bongiovanni M., Leroy F., Dalmasso A. Genetic variation in Meloidogyne incognita virulence against the tomato Mi resistance gene-evidence from isofemale line selection studies. Theor. Appl. Genet. 1994, 88:749-753.
14. Castagnone-Sereno P., Bongiovanni M., Palloix A., Dalmasso A. Selection for Meloidogyne incognita virulence against resistance genes from tomato and pepper and specificity of the virulence/resistance determinants. Eur. J. Plant Pathol. 1996, 102:585-590.
15. Castagnone-Sereno P., Semblat J.-P., Castagnone C. Modular architecture and evolution of the map-1 gene family in the root-knot nematode Meloidogyne incognita. Mol. Genet. Genomics 2009, 282:547-554.
16. Castagnone-Sereno P., Deleury E., Danchin E.G.J., Perfus-Barbeoch L., Abad P. Data-mining of the Meloidogyne incognita degradome and comparative analysis of proteases in nematodes. Genomics 2011, 97:29-36.
17. Cosgrove D.J. Growth of the plant cell wall. Nat. Rev. Mol. Cell Biol. 2005, 6:850-861.
18. Craig A., Ewan R., Mesmar J., Gudipati V., Sadanandom A. E3 ubiquitin ligases and plant innate immunity. J. Exp. Bot. 2009, 60:1123-1132.
19. Danchin E.G.J., et al. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. PNAS 2010, 107:17651-17656.
20. Dautova M., Rosso M.N., Abad P., Gommers F.J., Bakker J., Smant G. Single pass cDNA sequencing-a powerful tool to analyse gene expression in preparasitic juveniles of the southern root-knot nematode Meloidogyne incognita. Nematology 2001, 3:129-139.
21. Davis E.L., Hussey R.S., Baum T.J., Bakker J., Schots A. Nematode parasitism genes. Annu. Rev. Phytopathol. 2000, 38:365-396.
22. Davis E.L., Hussey R.S., Baum T.J. Getting to the roots of parasitism by nematodes. Trends Parasitol. 2004, 20:134-141.
23. de Boer J.M., et al. Developmental expression of secretory beta-1,4-endoglucanases in the subventral esophageal glands of Heterodera glycines. Mol. Plant Microbe Interact. 1999, 12:663-669.
24. de Boer J.M., et al. The use of DNA microarrays for the developmental expression analysis of cDNAs from the oesophageal gland cell region of Heterodera glycines. Mol. Plant Pathol. 2002, 3:261-270.
25. de Boer J.M., et al. Cloning of a putative pectate lyase gene expressed in the subventral esophageal glands of Heterodera glycines. J. Nematol. 2002, 34:9-11.
26. De Meutter J., Vanholme B., Bauw G., Tytgat T., Gheysen G., Gheysen G. Preparation and sequencing of secreted proteins from the pharyngeal glands of the plant parasitic nematode Heterodera schachtii. Mol. Plant Pathol. 2001, 2:297-301.
27. De Meutter J., Tytgat T., Witters E., Gheysen G., Van Onckelen H., Gheysen G. Identification of cytokinins produced by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Mol. Plant Pathol. 2003, 4:271-277.
28. De Meutter J., Tytgat T., Prinsen E., Gheysen G., Van Onckelen H., Gheysen G. Production of auxin and related compounds by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Commun. Agric. Appl. Biol. Sci. 2005, 70:51-60.
29. Ding X., Shields J., Allen R., Hussey R.S. A secretory cellulose-binding protein cDNA cloned from the root-knot nematode (Meloidogyne incognita). Mol. Plant Microbe Interact. 1998, 11:952-959.
30. Doyle E.A., Lambert K.N. Cloning and characterization of an esophageal-gland-specific pectate lyase from the root-knot nematode Meloidogyne javanica. Mol. Plant Microbe Interact. 2002, 15:549-556.
31. Doyle E.A., Lambert K.N. Meloidogyne javanica chorismate mutase 1 alters plant cell development. Mol. Plant Microbe Interact. 2003, 16:123-131.
32. Dubreuil G., Magliano M., Deleury E., Abad P., Rosso M.N. Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism. New Phytol. 2007, 176:426-436.
33. Dubreuil G., Deleury E., Magliano M., Jaouannet M., Abad P., Rosso M.N. Peroxiredoxins from the plant parasitic root-knot nematode, Meloidogyne incognita, are required for successful development within the host. Int. J. Parasitol. 2011, 41:385-396.
34. Elling A.A., et al. Sequence mining and transcript profiling to explore cyst nematode parasitism. BMC Genomics 2009, 10:58.
35. Endo B.Y. Feeding plug formation in soybean roots infected with the soy bean cyst nematode Heterodera glycines. J. Ultrastruct. Res. 1978, 72:349-366.
36. Erhardt D.W., Wais R., Long S.R. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 1996, 85:673-681.
37. Estelle M. Proteases and cellular regulation in plants. Curr. Opin. Plant Biol. 2001, 4:254-260.
38. Favery B., et al. The endosymbiosis-induced genes ENOD40 and CCS52a are involved in endoparasitic-nematode interactions in Medicago truncatula. Mol. Plant Microbe Interact. 2002, 15:1008-1013.
39. Fiers M., et al. The 14-Amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell 2005, 17:2542-2553.
40. Flor H.H. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 1971, 9:275-296.
41. Fujikawa T., Yamashita T., Tsuyumu S. Hypersensitive response suppression by type III effectors of plant pathogenic bacteria. J. Gen. Plant Pathol. 2006, 72:176-179.
42. Furlanetto C., Cardle L., Brown D.J.F., Jones J.T. Analysis of expressed sequence tags from the ectoparasitic nematode Xiphinema index. Nematology 2005, 7:95-104.
43. Gao B., Allen R., Maier T., Davis E.L., Baum T.J., Hussey R.S. Identification of a new beta-1,4-endoglucanase gene expressed in the esophageal subventral gland cells of Heterodera glycines. J. Nematol. 2002, 34:12-15.
44. Gao B., Allen R., Maier T., Davis E.L., Baum T.J., Hussey R.S. The parasitome of the phytonematode Heterodera glycines. Mol. Plant Microbe Interact. 2003, 16:720-726.
45. Gao B., Allen R., Davis E.L., Baum T.J., Hussey R.S. Molecular characterisation and developmental expression of a cellulose-binding protein gene in the soybean cyst nematode Heterodera glycines. Int. J. Parasitol. 2004, 34:1377-1383.
46. Gleason C.A., Liu Q.L., Williamson V.M. Silencing a candidate nematode effector gene corresponding to the tomato resistance gene Mi-1 leads to acquisition of virulence. Mol. Plant Microbe Interact. 2008, 21:576.
47. Goellner M., Smant G., de Boer J.M., Baum T.J., Davis E.L. Isolation of beta-1,4-endoglucanase genes from Globodera tabacum and their expression during parasitism. J. Nematol. 2000, 32:154-165.
48. Göhre V., et al. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 2008, 18:1824-1832.
49. Goverse A., Bird D. The role of plant hormones in nematode feeding site formation. Genomics and Molecular Genetics of Plant-Nematode Interactions 2011, 325-347. Springer, Heidelberg. J. Jones, G. Gheysen, C. Fenoll (Eds.).
50. Goverse A., et al. 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. 1999, 12:872-881.
51. Grundler F.M.W., Sobczak M., Golinowski W. Formation of wall openings in root cells of Arabidopsis thaliana following infection by the plant-parasitic nematode Heterodera schachtii. Eur. J. Plant Pathol. 1998, 104:545-551.
52. Grunewald W., Van Noorden G., Van Isterdael G., Beeckman T., Gheysen G., Mathesius U. Manipulation of auxin transport in plant roots during rhizobium symbiosis and nematode parasitism. Plant Cell 2009, 21:2553-2562.
53. Grunewald W., Cannoot B., Friml J., Gheysen G. Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog. 2009, 5:e1000266.
54. Guo Y., Ni J., Denver R., Wang X., Clark S.E. Mechanisms of molecular mimicry of plant CLE peptide ligands by the parasitic nematode Globodera rostochiensis. Plant Physiol. 2011, 157:476-484.
55. Haegeman A., Jacob J., Vanholme B., Kyndt T., Gheysen G. A family of GHF5 endo-1,4-beta-glucanases in the migratory plant-parasitic nematode Radopholus similis. Plant Pathol. 2008, 57:581-590.
56. Haegeman A., Jacob J., Vanholme B., Kyndt T., Mitreva M., Gheysen G. Expressed sequence tags of the peanut pod nematode Ditylenchus africanus: the first transcriptome analysis of an Anguinid nematode. Mol. Biochem. Parasitol. 2009, 167:32-40.
57. Haegeman A., Vanholme B., Gheysen G. Characterization of a putative endoxylanase in the migratory plant-parasitic nematode Radopholus similis. Mol. Plant Pathol. 2009, 10:389-401.
58. Haegeman A., Kyndt T., Gheysen G. The role of pseudo-endoglucanases in the evolution of nematode cell wall modifying proteins. J. Mol. Evol. 2010, 70:441-452.
59. Haegeman A., Joseph S., Gheysen G. Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Mol. Biochem. Parasitol. 2011, 178:7-14.
60. Haegeman A., Jones J.T., Danchin E.G.J. Horizontal gene transfer in nematodes: a catalyst for plant parasitism?. Mol. Plant Microbe Interact. 2011, 24:879-887.
61. Henkle-Duhrsen K., Kampkotter A. Antioxidant enzyme families in parasitic nematodes. Mol. Biochem. Parasitol. 2001, 114:129-142.
62. Hewezi T., et al. Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: Cooperative cell wall modification during parasitism. Plant Cell 2008, 20:3080-3093.
63. Hewezi T., et al. Arabidopsis spermidine synthase Is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol. 2010, 152:968-984.
64. Hirakawa Y., Kondo Y., Fukuda H. Regulation of vascular development by CLE peptide-receptor systems. J. Integr. Plant Biol. 2010, 52:8-16.
65. Hogenhout S.A., Van der Hoorn R.A.L., Terauchi R., Kamoun S. Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interact. 2009, 22:115-122.
66. Huang G.Z., et al. A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol. Plant Microbe Interact. 2003, 16:376-381.
67. Huang G.Z., Dong R.H., Allen R., Davis E.L., Baum T.J., Hussey R.S. Developmental expression and molecular analysis of two Meloidogyne incognita pectate lyase genes. Int. J. Parasitol. 2005, 35:685-692.
68. Huang G.Z., Dong R.H., Allen R., Davis E.L., Baum T.J., Hussey R.S. Two chorismate mutase genes from the root-knot nematode Meloidogyne incognita. Mol. Plant Pathol. 2005, 6:23-30.
69. Huang G.Z., Dong R.H., Allen R., Davis E.L., Baum T.J., Hussey R.S. A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol. Plant Microbe Interact. 2006, 19:463-470.
70. Huang G.Z., Allen R., Davis E.L., Baum T.J., Hussey R.S. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. PNAS 2006, 103:14302-14306.
71. Hussey R.S., Huang G., Allen R. Microaspiration of esophageal gland cells and cDNA library construction for identifying parasitism genes of plant-parasitic nematodes. Methods Mol. Biol. 2011, 712:89-107.
72. Ithal N., Recknor J., Nettleton D., Maier T., Baum T.J., Mitchum M.G. Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol. Plant Microbe Interact. 2007, 20:510-525.
73. Ito Y., et al. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 2006, 313:842-845.
74. Jacob J., Vanholme B., Haegeman A., Gheysen G. Four transthyretin-like genes of the migratory plant-parasitic nematode Radopholus similis: members of an extensive nematode-specific family. Gene 2007, 402:9-19.
75. Jacob J., Mitreva M., Vanholme B., Gheysen G. Exploring the transcriptome of the burrowing nematode Radopholus similis. Mol. Genet. Genomics 2008, 280:1-17.
76. Jasmer D.P., Goverse A., Smant G. Parasitic nematode interactions with mammals and plants. Annu. Rev. Phytopathol. 2003, 41:245-270.
77. Jaubert S., Ledger T.N., Laffaire J.B., Piotte C., Abad P., Rosso M.N. Direct identification of stylet secreted proteins from root-knot nematodes by a proteomic approach. Mol. Biochem. Parasitol. 2002, 121:205-211.
78. Jaubert S., Laffaire J.B., Abad P., Rosso M.N. A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Lett. 2002, 522:109-112.
79. Jones J.D.G., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
80. Jones M.G.K., Payne H.L. Early stage of nematode-induced giant-cell formation in roots of Impatiens balsamina. J. Nematol. 1978, 10:70-84.
81. Jones J.T., Smant G., Blok V.C. SXP/RAL-2 proteins of the potato cyst nematode Globodera rostochiensis: secreted proteins of the hypodermis and amphids. Nematology 2000, 2:887-893.
82. Jones J.T., et al. Characterization of a chorismate mutase from the potato cyst nematode Globodera pallida. Mol. Plant Pathol. 2003, 4:43-50.
83. Jones J.T., Reavy B., Smant G., Prior A.E. Glutathione peroxidases of the potato cyst nematode Globodera rostochiensis. Gene 2004, 324:47-54.
84. Jones J.T., Furlanetto C., Kikuchi T. Horizontal gene transfer from bacteria and fungi as a driving force in the evolution of plant parasitism in nematodes. Nematology 2005, 7:641-646.
85. Jones J.T., et al. 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. 2009, 10:815-828.
86. Jun J.H., et al. Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol. 2010, 154:1721-1736.
87. Kang M.J., Kim Y.H., Hahn B.S. Expressed sequence tag analysis generated from a normalized full-length cDNA library of the root-knot nematode (Meloidogyne incognita). Genes Genomics 2010, 32:553-562.
88. Karim N., Jones J.T., Okada H., Kikuchi T. Analysis of expressed sequence tags and identification of genes encoding cell-wall-degrading enzymes from the fungivorous nematode Aphelenchus avenae. BMC Genomics 2009, 10:525.
89. Kikuchi T., Jones J.T., Aikawa T., Kosaka H., Ogura N. A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. FEBS Lett. 2004, 572:201-205.
90. Kikuchi T., Shibuya H., Jones J.T. Molecular and biochemical characterization of an endo-beta-1,3-glucanase from the pinewood nematode Bursaphelenchus xylophilus acquired by horizontal gene transfer from bacteria. Biochem. J. 2005, 389:117-125.
91. Kikuchi T., Shibuya H., Aikawa T., Jones J.T. Cloning and characterization of pectate lyases expressed in the esophageal gland of the pine wood nematode Bursaphelenchus xylophilus. Mol. Plant Microbe Interact. 2006, 19:280-287.
92. Kikuchi T., Aikawa T., Kosaka H., Pritchard L., Ogura N., Jones J.T. Expressed sequence tag (EST) analysis of the pine wood nematode Bursaphelenchus xylophilus and B. mucronatus. Mol. Biochem. Parasitol. 2007, 155:9-17.
93. Kikuchi T., Li H.M., Karim N., Kennedy M.W., Moens M., Jones J.T. Identification of putative expansin-like genes from the pine wood nematode, Bursaphelenchus xylophilus, and evolution of the expansin gene family within the Nematoda. Nematology 2009, 11:355-364.
94. Kikuchi T., et al. Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathog. 2011, 7:e1002219.
95. Kondo Y., Hirakawa Y., Kieber J.J., Fukuda H. CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling. Plant Cell Physiol. 2011, 52:37-48.
96. Kudla U., et al. Origin, distribution and 3D-modeling of Gr-EXPB1, an expansin from the potato cyst nematode Globodera rostochiensis. FEBS Lett. 2005, 579:2451-2457.
97. Kumar S., Blaxter M. The 959 nematode genomes initiative Accessed 30 September 2011. http://www.nematodes.org/nematodegenomes/.
98. Kunkel B.N., Brooks D.M. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 2002, 5:325-331.
99. Kvitko B.H., et al. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog. 2009, 5:e1000388.
100. Lamb C., Dixon R.A. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997, 48:251-275.
101. Lambert K.N., Allen K.D., Sussex I.M. Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica. Mol. Plant Microbe Interact. 1999, 12:328-336.
102. Ledger T.N., Jaubert S., Bosselut N., Abad P., Rosso M.N. Characterization of a new beta-1,4-endoglucanase gene from the root-knot nematode Meloidogyne incognita and evolutionary scheme for phytonematode family 5 glycosyl hydrolases. Gene 2006, 382:121-128.
103. Lee C., et al. The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiol. 2011, 155:866-880.
104. Lee H., Chah O.K., Sheen J. Stem-cell-triggered immunity through CLV3p-FLS2 signalling. Nature 2011, 473:376-U559.
105. Lohar D.P., Bird D.M. Lotus japonicus: a new model to study root-parasitic nematodes. Plant Cell Physiol. 2003, 44:1176-1184.
106. Long H., Wang X., Xu J. Molecular cloning and life-stage expression pattern of a new chorismate mutase gene from the root-knot nematode Meloidogyne arenaria. Plant Pathol. 2006, 55:559-563.
107. Lu S.-W., Tian D., Borchardt-Wier H.B., Wang X. Alternative splicing: a novel mechanism of regulation identified in the chorismate mutase gene of the potato cyst nematode Globodera rostochiensis. Mol. Biochem. Parasitol. 2008, 162:1-15.
108. Lu S.W., et al. Structural and functional diversity of CLAVATA3/ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis. Mol. Plant Microbe Interact. 2009, 22:1128-1142.
109. Martin K., Kopperud K., Chakrabarty R., Banerjee R., Brooks R., Goodin M.M. Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant J. 2009, 59:150-162.
110. Mbeunkui F., Scholl E.H., Opperman C.H., Goshe M.B., Bird D.M. Proteomic and bioinformatic analysis of the root-knot nematode Meloidogyne hapla: the basis for plant parasitism. J. Proteome Res. 2010, 9:5370-5381.
111. McCarter J.P., et al. Analysis and functional classification of transcripts from the nematode Meloidogyne incognita. Genome Biol. 2003, 4:R26.
112. Mitchum M.G., Wang X.H., Davis E.L. Diverse and conserved roles of CLE peptides. Curr. Opin. Plant Biol. 2008, 11:75-81.
113. Mitreva M., et al. A survey of SL1-spliced transcripts from the root-lesion nematode Pratylenchus penetrans. Mol. Genet. Genomics 2004, 272:138-148.
114. Mitreva-Dautova M., et al. A symbiont-independent endo-1,4-beta-xylanase from the plant-parasitic nematode Meloidogyne incognita. Mol. Plant Microbe Interact. 2006, 19:521-529.
115. Miwa H., Betsuyaku S., Iwamoto K., Kinoshita A., Fukuda H., Sawa S. The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol. 2008, 49:1752-1757.
116. Miwa H., Kinoshita A., Fukuda H., Sawa S. Plant meristems: CLAVATA3/ESR-related signaling in the shoot apical meristem and the root apical meristem. J. Plant Res. 2009, 122:31-39.
117. Moons A. Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTS). Vitam. Horm. 2005, 72:155-202.
118. Nagano I., Wu Z.L., Takahashi Y. Functional genes and proteins of Trichinella spp. Parasitol. Res. 2009, 104:197-207.
119. Nam K.H., Li J.M. The Arabidopsis transthyretin-like protein is a potential substrate of BRASSINOSTEROID-INSENSITIVE 1. Plant Cell 2004, 16:2406-2417.
120. Neveu C., Abad P., Castagnone-Sereno P. Molecular cloning and characterization of an intestinal cathepsin L protease from the plant-parasitic nematode Meloidogyne incognita. Physiol. Mol. Plant Pathol. 2003, 63:159-165.
121. Ni J., Clark S.E. Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain. Plant Physiol. 2006, 140:726-733.
122. Oelkers K., Goffard N., Weiller G.F., Gresshoff P.M., Mathesius U., Frickey T. Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biol. 2008, 8:1.
123. Oh H.S., Collmer A. Basal resistance against bacteria in Nicotiana benthamiana leaves is accompanied by reduced vascular staining and suppressed by multiple Pseudomonas syringae type III secretion system effector proteins. Plant J. 2005, 44:348-359.
124. Ohyama K., Ogawa M., Matsubayashi Y. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J. 2008, 55:152-160.
125. Opperman C.H., et al. Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. PNAS 2008, 105:14802-14807.
126. Palha J.A. Transthyretin as a thyroid hormone carrier: function revisited. Clin. Chem. Lab. Med. 2002, 40:1292-1300.
127. Patel N., et al. Similarity and functional analyses of expressed parasitism genes in Heterodera schachtii and Heterodera glycines. J. Nematol. 2008, 40:299-310.
128. Patel N., et al. A nematode effector protein similar to annexins in host plants. J. Exp. Bot. 2010, 61:235-248.
129. Perry R.N. Chemoreception in plant parasitic nematodes. Annu. Rev. Phytopathol. 1996, 34:181-199.
130. Petrasek J., Friml J. Auxin transport routes in plant development. Development 2009, 136:2675-2688.
131. Popeijus M., et al. Analysis of genes expressed in second stage juveniles of the potato cyst nematodes Globodera rostochiensis and G. pallida using the expressed sequence tag approach. Nematology 2000, 2:567-574.
132. Popeijus H., et al. Enzymology-degradation of plant cell walls by a nematode. Nature 2000, 406:36-37.
133. Premachandran D., Vonmende N., Hussey R.S., Mcclure M.A. A method for staining nematode secretions and structures. J. Nematol. 1988, 20:70-78.
134. Prior A., et al. 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. 2001, 356:387-394.
135. Pritchard L., Birch P. A systems biology perspective on plant-microbe interactions: biochemical and structural targets of pathogen effectors. Plant Sci. 2011, 180:584-603.
136. Qin L., et al. An efficient cDNA-AFLP-based strategy for the identification of putative pathogenicity factors from the potato cyst nematode Globodera rostochiensis. Mol. Plant Microbe Interact. 2000, 13:830-836.
137. Qin L., et al. Plant degradation: a nematode expansin acting on plants. Nature 2004, 427:30.
138. Rehman S., et al. Identification and characterization of the most abundant cellulases in stylet secretions from Globodera rostochiensis. Phytopathology 2009, 99:194-202.
139. Rehman S., et al. A secreted SPRY domain-containing protein (SPRYSEC) from the plant-parasitic nematode Globodera rostochiensis interacts with a CC-NB-LRR protein from a susceptible tomato. Mol. Plant Microbe Interact. 2009, 22:330-340.
140. Reid D., Ferguson B.J., Gresshoff P.M. Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol. Plant Microbe Interact. 2011, 24:606-618.
141. Replogle A., et al. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. Plant J. 2011, 65:430-440.
142. Robertson L., Robertson W.M., Jones J.T. Direct analysis of the secretions of the potato cyst nematode Globodera rostochiensis. Parasitology 1999, 119:167-176.
143. Robertson L., et al. Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis. Mol. Biochem. Parasitol. 2000, 111:41-49.
144. Robinson M.P., Atkinson H.J., Perry R.N. The association and partial characterisation of a fluorescent hypersensitive response of potato roots to the potato cyst nematodes Globodera rostochiensis and G. pallida. Rev. Nematol. 1988, 11:99-107.
145. Rojo E., Sharma V.K., Kovaleva V., Raikhel N.V., Fletcher J.C. CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 2002, 14:969-977.
146. Rosso M.N., et al. Isolation of a cDNA encoding a beta-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Mol. Plant Microbe Interact. 1999, 12:585-591.
147. Roze E., Hanse B., Mitreva M., Vanholme B., Bakker J., Smant G. Mining the secretome of the root-knot nematode Meloidogyne chitwoodi for candidate parasitism genes. Mol. Plant Pathol. 2008, 9:1-10.
148. Sacco M.A., et al. The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2-and RanGAP2-dependent plant cell death. PLoS Pathog. 2009, 5:e1000564.
149. Scholl E.H., Thorne J.L., McCarter J.P., Bird D.M. Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. Genome Biol. 2003, 4:R39.
150. Semblat J.P., Rosso M.N., Hussey R.S., Abad P., Castagnone-Sereno P. Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita. Mol. Plant Microbe Interact. 2001, 14:72-79.
151. Smant G., Jones J.T. Suppression of plant defences by nematodes. Genomics and Molecular Genetics of Plant-Nematode Interactions 2011, 273-286. Springer, Heidelberg. J.T. Jones, G. Gheysen, C. Fenoll (Eds.).
152. Smant G., et al. Endogenous cellulases in animals: Isolation of beta-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. PNAS 1998, 95:4906-4911.
153. Spiegel Y., Mcclure M.A. The surface coat of plant-parasitic nematodes-chemical composition, origin, and biological role-a review. J. Nematol. 1995, 27:127-134.
154. Spiegel Y., Kahane I., Cohen L., Sharon E. Meloidogyne javanica surface proteins: characterization and lability. Parasitology 1997, 115:513-519.
155. Stahl Y., Wink R.H., Ingram G.C., Simon R. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 2009, 19:909-914.
156. Stewart G.R., Perry R.N., Wright D.J. Studies on the amphid specific glycoprotein Gp32 in different life cycle stages of Meloidogyne species. Parasitology 1993, 107:573-578.
157. Swarup K., et al. The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 2008, 10:946-954.
158. Thomma B.P.H.J., et al. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. PNAS 1998, 95:15107-15111.
159. Truchet G., et al. Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfafa. Nature 1991, 351:670-673.
160. Tytgat T., et al. A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant parasitic cyst nematodes. Mol. Plant Microbe Interact. 2004, 17:846-852.
161. Uehara T., Kushida A., Momota Y. PCR-based cloning of two beta-1,4-endoglucanases from the root-lesion nematode Pratylenchus penetrans. Nematology 2001, 3:335-341.
162. Urwin P.E., Lilley C.J., McPherson M.J., Atkinson H.J. Characterization of two cDNAs encoding cysteine proteinases from the soybean cyst nematode Heterodera glycines. Parasitology 1997, 114:605-613.
163. van der Biezen E.A., Jones J.D.G. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 1998, 23:454-456.
164. van Megen H., et al. A phylogenetic tree of nematodes based on about 1200 full length small subunit ribosomal DNA sequences. Nematology 2009, 11:927-950.
165. Vanholme B., et al. Detection of putative secreted proteins in the plant-parasitic nematode Heterodera schachtii. Parasitol. Res. 2006, 98:414-424.
166. Vanholme B., Van Thuyne W., Vanhouteghem K., De Meutter J., Cannoot B., Gheysen G. Molecular characterization and functional importance of pectate lyase secreted by the cyst nematode Heterodera schachtii. Mol. Plant Pathol. 2007, 8:267-278.
167. Vanholme B., Haegeman A., Jacob J., Cannoot B., Gheysen G. Arabinogalactan endo-1,4-beta-galactosidase: a putative plant cell wall-degrading enzyme of plant-parasitic nematodes. Nematology 2009, 11:739-747.
168. Vanholme B., Kast P., Haegeman A., Jacob J., Grünewald W., Gheysen G. Structural and functional investigation of a secreted chorismate mutase from the plant-parasitic nematode Heterodera schachtii in the context of related enzymes from diverse origins. Mol. Plant Pathol. 2009, 10:189-200.
169. Verdejo-Lucas S., Cortada L., Sorribas F.J., Ornat C. Selection of virulent populations of Meloidogyne javanica by repeated cultivation of Mi resistance gene tomato rootstocks under field conditions. Plant Pathol. 2009, 58:990-998.
170. Vieira P., et al. The plant apoplasm is an important recipient compartment for nematode secreted proteins. J. Exp. Bot. 2011, 62:1241-1253.
171. Waetzig G.H., Sobczak M., Grundler F.M.W. Localization of hydrogen peroxide during the defence response of Arabidopsis thaliana against the plant-parasitic nematode Heterodera glycines. Nematology 1999, 1:681-686.
172. Wang X., et al. In planta localization of a beta-1,4-endoglucanase secreted by Heterodera glycines. Mol. Plant Microbe Interact. 1999, 12:64-67.
173. Wang X., et al. Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant Microbe Interact. 2001, 14:536-544.
174. Wang X., et al. A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol. Plant Pathol. 2005, 6:187-191.
175. Wang J., et al. Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytol. 2010, 187:1003-1017.
176. Wang J., Joshi S., Korkin D., Mitchum M.G. Variable domain I of nematode CLEs directs post-translational targeting of CLE peptides to the extracellular space. Plant Signal. Behav. 2010, 5:1-3.
177. Wang J., et al. Identification of potential host plant mimics of CLAVATA3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii. Mol. Plant Pathol. 2011, 12:177-186.
178. Wasmuth J., Schmid R., Hedley A., Blaxter M. On the extent and origins of genic novelty in the phylum Nematoda. PLoS Negl. Trop. Dis. 2008, 2.
179. Weerasinghe R.R., Collings D.A., Johannes E., Allen N.S. The distributional changes and role of microtubules in Nod factor-challenged Medicago sativa root hairs. Planta 2003, 218:276-287.
180. Weerasinghe R.R., Bird D.M., Allen N.S. Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. PNAS 2005, 102:3147-3152.
181. Whitford R., Fernandez A., De Groodt R., Ortega E., Hilson P. Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. PNAS 2008, 105:18625-18630.
182. Wildermuth M.C., Dewdney J., Wu G., Ausubel F.M. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 2001, 414:562-565.
183. Williamson V.M., Hussey R.S. Nematode pathogenesis and resistance in plants. Plant Cell 1996, 8:1735-1745.
184. Wubben M.J., Callahan F.E., Scheffler B.S. Transcript analysis of parasitic females of the sedentary semi-endoparasitic nematode Rotylenchulus reniformis. Mol. Biochem. Parasitol. 2010, 172:31-40.
185. Wubben M.J., Callahan F.E. Isolation and characterization of a GHF5 beta-1,4-endoglucanase from the reniform nematode (Rotylenchulus reniformis). J. Nematol. 2010, 42:276-277.
186. Wuyts N., Swennen R., De Waele D. Effects of plant phenylpropanoid pathway products and selected terpenoids and alkaloids on the behaviour of the plant-parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne incognita. Nematology 2006, 8:89-101.
187. Wuyts N., Lognay G., Verscheure M., Marlier M., De Waele D., Swennen R. Potential physical and chemical barriers to infection by the burrowing nematode Radopholus similis in roots of susceptible and resistant banana (Musa spp.). Plant Pathol. 2007, 56:878-890.
188. Yan Y.T., et al. Genomic organization of four beta-1,4-endoglucanase genes in plant-parasitic cyst nematodes and its evolutionary implications. Gene 1998, 220:61-70.
189. Yan Y.T., Smant G., Davis E. Functional screening yields a new beta-1,4-endoglucanase gene from Heterodera glycines that may be the product of recent gene duplication. Mol. Plant Microbe Interact. 2001, 14:63-71.