Abstract
Like microbial pathogens, nematodes secrete a repertoire of effectors with diverse functions. In the case of sedentary nematodes, completion of the life cycle requires the maintenance of the biotrophic interaction for several weeks and the induction of a permanent feeding site. These essential processes require fine tuning of plant cell responses. About a hundred candidate effectors have been isolated from nematodes to date that have roles in the invasion of host tissues, evasion of plant defences, suppression of plant defences or manipulation of plant cell fate. Evolutionary studies suggest that several distinct mechanisms have led to the acquisition of these effectors during the evolution of plant parasitism. In addition, since any compound secreted by the parasite can potentially be perceived as nonself by the plant, nematode effectors are subject to selective pressure to escape plant immunity. This chapter reviews the latest findings on nematode effector functions and evolutionary traits.
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References
Abad P, Gouzy J, Aury J-M, Castagnone-Sereno P, Danchin EGJ et al (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26:909–915
Agrawal GK, Jwa N-S, Lebrun M-H, Job D, Rakwal R (2010) Plant secretome: unlocking secrets of the secreted proteins. Proteomics 10:799–827
Aguileta G, Refrégier G, Yockteng R, Fournier E, Giraud T (2009) Rapidly evolving genes in pathogens: methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Infect Genet Evol 9:656–670
Antelmann H, Tjalsma H, Voigt B, Ohlmeier S, Bron S et al (2001) A proteomic view on genome-based signal peptide predictions. Genome Res 11:1484–502
Baker C, Orlandi E (1995) Active oxygen in plant pathogenesis. Ann Rev Phytopathol 33:299–321
Bekal S, Niblack TL, Lambert KN (2003) A chorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence. Mol Plant-Mic Interact 16:439–446
Bellafiore S, Shen Z, Rosso MN, Abad P, Shih P, Briggs S (2008) Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathog 4:e1000192
Bird A (1968) Changes associated with parasitism in nematodes. III. Ultrastructure of the egg shell, larval cuticle, and contents of the subventral esophageal glands in Meloidogyne javanica, with some observations on hatching. J Parasitol 54:475–489
Bird A (1969) Changes associated with parasitism in nematodes. V. Ultrastructure of the stylet exudation and dorsal esophageal gland contents of female Meloidogyne javanica. J Parasitol 55:337–345
Blanchard A, Esquibet M, Fouville D, Grenier E (2005) Ranbpm homologue genes characterised in the cyst nematodes Globodera pallida and Globodera mexicana. Physiol Mol Plant Pathol 67:15–22
Blanchard A, Fouville D, Esquibet M, Mugniéry D, Grenier E (2007) Sequence polymorphism of 2 pioneer genes expressed in phytoparasitic nematodes showing different host ranges. J Heredity 98:611–619
Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P et al (1998) A molecular evolutionary framework for the phylum Nematoda. Nature Biotechnol 392:71–75
Borisjuk N, Sitailo L, Adler K, Malysheva L, Tewes A, Borisjuk L, Manteuffel R (1998) Calreticulin expression in plant cells: developmental regulation, tissue specificity and intracellular distribution. Planta 206:504–514
Castagnone-Sereno P, Semblat JP, Castagnone C (2009) Modular architecture and evolution of the map-1 gene family in the root-knot nematode Meloidogyne incognita. Mol Gen Genom 282:547–554
Chisholm S, Coaker G, Day B, Staskawicz B (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814
Craig JP, Bekal S, Hudson M, Domier L, Niblack T, Lambert KN (2008) Analysis of a horizontally transferred pathway involved in vitamin B6 biosynthesis from the soybean cyst nematode Heterodera glycines. Mol Biol Evol 25:2085–2098
Curtis RHC (2007) Plant parasitic nematode proteins and the host parasite interaction. Brief Funct Genomic Proteomic 6:50–58
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 U S A 107:17651–17656
Davis EL, Hussey RS, Baum TJ, Bakker J, Schots A et al (2000) Nematode parasitism genes. Ann Rev Phytopathol 38:365–396
De Meutter J, Vanholme B, Bauw G, Tytgat T, Gheysen G (2001) Preparation and sequencing of secreted proteins from the pharyngeal glands of the plant parasitic nematode Heterodera schachtii. Mol Plant Pathol 2:297–301
De Meutter J, Tytgat T, Prinsen E, Van Onckelen H, Gheysen G (2005) Production of auxin and related compounds by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Comm Ag App Biol Sci 70:51–60
De Verdal H, Fournet S, Grenier E, Petit E (2009) Pathogenicity gene polymorphism in H. schachtii: molecular evidence for local adaptation? In: Proceedings of the 3rd Annual Meeting of the COST 872, Toledo, Spain, 2009
Denver DR, Dolan PC, Wilhelm LJ, Sung W, Lucas-Lledo JI et al (2009) A genome-wide view of Caenorhabditis elegans base-substitution mutation processes. Proc Natl Acad Sci U S A 106:16310–16314
Doyle E, Lambert K (2002) Cloning and characterisation of an esophageal-gland specific pectate lyase from the root-knot nematode Meloidogyne javanica. Mol Plant-Mic Interact 15:549–556
Doyle EA, Lambert KN (2003) Meloidogyne javanica Chorismate Mutase 1 Alters Plant Cell Development. Mol Plant-Mic Interact 16:123–131
Dubreuil G, Magliano M, Deleury E, Abad P, Rosso MN (2007) Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism. New Phytol 176:426–436
Elling A, Davis E, Hussey R, Baum T (2007) Active uptake of cyst nematode parasitism proteins into the plant cell nucleus. Int J Parasitol 37:1269–1279
Elling A, Mitreva M, Gai X, Martin J, Recknor J et al (2009) Sequence mining and transcript profiling to explore cyst nematode parasitism. BMC Genomics 10:58
Endo BY (1978) Feeding plug formation in soybean roots infected with the soybean cyst nematode. Phytopathology 68:1022–1031
Fioretti L, Warry A, Porter A, Haydock P, Curtis R (2001) Isolation and localisation of an annexin gene (gp-nex) from the potato cyst nematode, Globodera pallida. Nematology 3:45–54
Gao B, Allen R, Maier T, Davis E, Baum T, Hussey R (2001) Molecular characterisation and expression of two venom allergen-like protein genes in Heterodera glycines. Int J Parasitol 31:1617–1625
Gao B, Allen R, Maier T, Davis E, Baum T, Hussey R (2003) The parasitome of the phytonematode Heterodera glycines. Mol Plant-Mic Interact 16:720–726
Garofalo A, Rowlinson M-C, Amambua NA, Hughes JM, Kelly SM et al (2003) The FAR Protein Family of the Nematode Caenorhabditis elegans. Differential lipid binding properties, structural characteristics and developmental regulation. J Biol Chem 278:8065–8074
Ghiran I, Klickstein LB, Nicholson-Weller A (2003) Calreticulin is at the surface of circulating neutrophils and uses CD59 as an adaptor molecule. J Biol Chem 278:21024–21031
Gleason CA, Liu QLL, Williamson VM (2008) Silencing a candidate nematode effector gene corresponding to the tomato resistance gene Mi-1 leads to acquisition of virulence. Mol Plant-Mic Interact 21:576–585
Goverse A, van der Voort JR, van der Voort CR, Kavelaars A, Smant G et al (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 12:872–881
Grunewald W, van Noorden G, Van Isterdael G, Beeckman T, Gheysen G, Mathesius U (2009) Manipulation of auxin transport in plant roots during Rhizobium symbiosis and nematode parasitism. Plant Cell 21:2553–2562
Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between Protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730
Haegeman A, Jacob J, Vanholme B, Kyndt T, Gheysen G (2008) A family of GHF5 endo-1,4-beta-glucanases in the migratory plant-parasitic nematode Radopholus similis. Plant Pathology 57:581–590
Haegeman A, Jacob J, Vanholme B, Kyndt T, Mitreva M, Gheysen G (2009) Expressed sequence tags of the peanut pod nematode Ditylenchus africanus: the first transcriptome analysis of an Anguinid nematode. Mol Biochem Parasitol 167:32–40
Hewezi T, Howe P, Maier T, Hussey R, Mitchum M et al (2008) Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20:3080–3093
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 152:968–984
Him N, Gillan V, Emes R, Maitland K, Devaney E (2009) Hsp-90 and the biology of nematodes. BMC Evol Biol 9:254
Hogenhout SA, Van der Hoorn RAL, Terauchi R, Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant-Mic Interact 22:115–122
Holterman MA, van der Wurff A, van den Elsen S, van Megen H, Bongers T et al (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol Biol Evol 23:1792–1800
Huang G, Gao B, Maier T, Allen R, Davis EL et al (2003) A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol Plant-Mic Interact 16:376–381
Huang G, Allen R, Davis EL, Baum TJ, Hussey RS (2006a) Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc Natl Acad Sci U S A 103:14302–14306
Huang GZ, Dong RH, Allen R, Davis EL, Baum TJ, Hussey RS (2006b) A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Molecular Plant-Microbe Interactions 19:463–470
Hunt PW, McNally J, Barris W, Blaxter M (2009) Duplication and divergence: The evolution of nematode globins. J Nematol 41:35–51
Hussey RS (1989) Disease-inducing secretions of plant-parasitic nematodes. Ann Rev Phytopathol 27:123–141
Ithal N, Recknor J, Nettleton D, Hearne L, Maier T et al (2007) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol Plant-Mic Interact 20:293–305
Jacob J, Vanholme B, Haegeman A, Gheysen G (2007). Four transthyretin-like genes of the migratory plant-parasitic nematode Radopholus similis: members of an extensive nematode-specific family. Gene 402:9–19
Jaubert S, Ledger TN, Laffaire JB, Piotte C, Abad P, Rosso MN (2002) Direct identification of stylet secreted proteins from root-knot nematodes by a proteomic approach. Mol Biochem Parasitol 121:205–211
Jaubert S, Laffaire JB, Ledger TN, Escoubas P, Amri EZ et al (2004) Comparative analysis of two 14-3-3 homologues and their expression pattern in the root-knot nematode Meloidogyne incognita. Int J Parasitol 34:873–880
Jaubert S, Milac AL, Petrescu J, de Almeida-Engler J, Abad P, Rosso MN (2005) In planta secretion of a calreticulin by migratory and sedentary stages of root-knot nematode. Mol Plant Microbe Interact 18:1277–1284
Jones JT, Perry R, Johnston M (1994) Changes in the ultrastructure of the amphids of the potato cyst nematode, Globodera rostochiensis, during development and infection. Fund App Nematol 17:369–382
Jones JT, Smant G, Blok VC (2000) SXP/RAL-2 proteins of the potato cyst nematode Globodera rostochiensis: secreted proteins of the hypodermis and amphids. Nematology 2:887–893
Jones JT, Furlanetto C, Bakker E, Banks B, Blok VC et al (2003) Characterization of a chorismate mutase from the potato cyst nematode Globodera pallida. Mol Plant Pathol 4:43–50
Jones JT, Reavy B, Smant G, Prior AE (2004) Glutathione peroxidases of the potato cyst nematode Globodera rostochiensis. Gene 324:47–54
Jones JT, Kumar A, Pylypenko LA, Thirugnanasambandam A, Castelli L, Chapman S, Cock PJA, Grenier E, Lilley CJ, Phillips MS, Blok VC (2009) Identification and functional characterization of effectors in expressed sequence tags from various life cycle stages of the potato cyst nematode Globodera pallida. Mol Plant Pathol 10:815–828
Kikuchi T, Aikawa T, Kosaka H, Pritchard L, Ogura N, Jones JT (2007) Expressed sequence tag (EST) analysis of the pine wood nematode Bursaphelenchus xylophilus and B. mucronatus. Mol Biochem Parasitol 155:9–17
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 14:1168–1177
Kyndt T, Haegeman A, Gheysen G (2008) Evolution of GHF5 endoglucanase gene structure in plant-parasitic nematodes: no evidence for an early domain shuffling event. BMC Evol Biol 8:305
Lambert KN, Allen KD, Sussex IM (1999) Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica. Mol Plant Microbe Interact 12:328–336
Lambert K, Bekal S, Domier L, Niblack T, Noel G, Smyth C (2005) Selection of Heterodera glycines chorismate mutase-1 alleles on nematode-resistant soybean. Mol Plant-Mic Interact 18:593–601
Ledger TN, Jaubert S, Bosselut N, Abad P, Rosso MN (2006) 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 382:121–128
Lee C, Chronis D, Kenning C, Peret B, Hewezi T, Davis EL, Baum TJ, Hussey R, Bennett M, Mitchum MG (2010) The Novel Cyst Nematode Effector Protein 19C07 Interacts with the Arabidopsis Auxin Influx Transporter LAX3 to Control Feeding Site Development. Plant Physiol. doi: 10.1104/pp.110.167197
Lu SW, Tian D, Borchardt-Wier HB, Wang X (2008) Alternative splicing: A novel mechanism of regulation identified in the chorismate mutase gene of the potato cyst nematode Globodera rostochiensis. Mol Biochem Parasitol 162:1–15
Lu SW, Chen S, Wang J, Yu H, Chronis D et al (2009) Structural and functional diversity of CLAVATA3/ESR (CLE)-Like genes from the potato cyst nematode Globodera rostochiensis. Mol Plant Microbe Interact 22:1128–1142
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155
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 Phytologist 170:501–512
Mueller CA, Broz P, Cornelis GR (2008) The type III secretion system tip complex and translocon. Mol Microbiol 68:1085–1095
Nagaraj SH, Gasser RB, Ranganathan S (2008) Needles in the EST haystack: Large-scale identification and analysis of excretory-secretory (ES) proteins in parasitic nematodes using Expressed Sequence Tags (ESTs). PLoS Negl Trop Dis 2:e301
Naresha S, Suryawanshi A, Agarwal M, Singh BP, Joshi P (2009) Mapping the complement C1q binding site in Haemonchus contortus calreticulin. Mol Biochem Parasitol 166:42–46
Nilsen TW, Graveley BR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature Biotech 463:457–463
Oecking C, Jaspert N (2009) Plant 14-3-3 proteins catch up with their mammalian orthologs. Curr Opin Plant Biol 12:760–765
Oladiran A, Belosevic M (2009) Trypanosoma carassii calreticulin binds host complement component C1q and inhibits classical complement pathway-mediated lysis. Dev Comp Immunol 34:396–405
Patel N, Hamamouch N, Li C, Hewezi T, Hussey RS et al (2010). A nematode effector protein similar to annexins in host plants. J Exp Bot 61:235–248
Perry RN (1996) Chemoreception in plant parasitic nematodes. Ann Rev Phytopathol 34:181–199
Petit E, Valette S (2008) Mitochondrial sequence heteroplasmy in the genus Globodera. In: Proceedings of the 2nd Annual Meeting of COST 872 Action. Postojna, Slovenia
Picard D, Sempere T, Plantard O (2007) A northward colonisation of the Andes by the potato cyst nematode during geological times suggests multiple host-shifts from wild to cultivated potatoes. Mol Phylogen Evol 42:308–316
Pouttu R, Puustinen T, Virkola R, Hacker J, Klemm P, Korhonen T (1999) Amino acid residue Ala-62 in the FimH fimbrial adhesin is critical for the adhesiveness of meningitis-associated Escherichia coli to collagens. Mol Microbiol 31:1747–1757
Prior A, Jones JT, Blok VC, Beauchamp J, McDermott L et al (2001) A surface-associated retinol- and fatty acid-binding protein (Gp-FAR-1) from the potato cyst nematode Globodera pallida: lipid binding activities, structural analysis and expression pattern. Biochem J 356:387–394
Ranganathan S, Menon R, Gasser RB (2009) Advanced in silico analysis of expressed sequence tag (EST) data for parasitic nematodes of major socio-economic importance—Fundamental insights toward biotechnological outcomes. Biotechnol Adv 27:439–448
Rehman S, Postma W, Tytgat T, Prins P, Qin L et al (2009a) 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 22:330–340
Rehman S, Butterbach P, Popeijus H, Overmars H, Davis EL et al (2009b) Identification and characterization of the most abundant cellulases in stylet secretions from Globodera rostochiensis. Phytopathology 99:194–202
Robertson L, Robertson WM, Jones JT (1999) Direct analysis of the secretions of the potato cyst nematode Globodera rostochiensis. Parasitology 119:167–176
Robertson L, Robertson WM, Sobczak M, Helder J, Tetaud E et al (2000) Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis. Mol Biochem Parasitol 111:41–49
Rosso MN, Jones JT, Abad P (2009) RNAi and functional genomics in plant parasitic nematodes: tools and discoveries in the post-genomic era. Ann Rev Phytopathol 47:207–232
Roze E, Hanse B, Mitreva M, Vanholme B, Bakker J, Smant G (2008) Mining the secretome of the root-knot nematode Meloidogyne chitwoodi for candidate parasitism genes. Mol Plant Pathol 9:1–10
Rzepecka J, Rausch S, Klotz C, Schnöller C, Kornprobst T et al (2009) Calreticulin from the intestinal nematode Heligmosomoides polygyrus is a Th2-skewing protein and interacts with murine scavenger receptor-A. Mol Immunol 46:1109–1119
Sacco MA, Koropacka K, Grenier E, Jaubert MJ, Blanchard A et al (2009) The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathog 5:e1000564
Scholl EH, Thorne JL, McCarter JP, Bird DM (2003) Horizontaly transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. Genome Biol 4:R39.1–12
Semblat J-P, Rosso M-Nl, Hussey RS, Abad P, Castagnone-Sereno P (2001) Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the Root-Knot nematode Meloidogyne incognita. Mol Plant Microbe Interact 14:72–79
Sharon E, Spiegel Y, Salomon R, Curtis RH (2002). Characterization of Meloidogyne javanica surface coat with antibodies and their effect on nematode behaviour. Parasitology 125:177–185
Shin C, Manley JL (2004) Cell signalling and the control of pre-mRNA splicing. Nat Rev Mol Cell Biol 5:727–738
Shindo T, Van der Hoorn RAL (2008) Papain-like cysteine proteases: key players at molecular battlefields employed by both plants and their invaders. Mol Plant Pathol 9:119–125
Simonetti E, Veronico P, Melillo MT, Delibes A, Andrés MF, López-Braña I (2009) Analysis of Class III peroxidase genes expressed in roots of resistant and susceptible wheat lines infected by Heterodera avenae. Mol Plant Microbe Interact 22:1081–1092
Smant G, Stokkerman JPWG, Yan Y, de Boer JM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J (1998) Endogenous cellulases in animals: Isolation of β-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci U S A. 95:4906–4911
Sobczak M, Golinowski W, Grundler F (1999) Ultrastructure of feeding plugs and feeding tubes formed by Heterodera schachtii. Nematology 1:363–374
Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR et al (2003) The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 1:e45
Tytgat T, Vanholme B, De Meutter J, Claeys M, Couvreur M et al (2004) A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant parasitic cyst nematodes. Mol Plant Microbe Interact 17:846–852
Tytgat T, Vercauteren I, Vanholme B, De Meutter J, Vanhoutte I et al (2005) An SXP/RAL-2 protein produced by the subventral pharyngeal glands in the plant parasitic root-knot nematode Meloidogyne incognita. Parasitol Res 95:50–54
van Megen H, van den Elsen S, Holterman M, Karssen G, Mooyman P et al (2009). A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11:927–950
Vanholme B, Mitreva M, Van Criekinge W, Logghe M, Bird D et al (2006) Detection of putative secreted proteins in the plant-parasitic nematode Heterodera schachtii. Parasitol Res 98:414–424
Veronico P, Jones J, DiVito M, De Giorgi C (2001) Horizontal transfer of a bacterial gene involved in polyglutamate biosynthesis to the plant-parasitic nematode Meloidogyne artiellia. FEBS Lett 508:470–474
Vieira P, Danchin EG, Neveu C, Crozat C, Jaubert S, Hussey RS, Engler G, Abad P, de Almeida-Engler J, Castagnone-Sereno P, Rosso MN (2010) The plant apoplasm is an important recipient compartment for nematode secreted proteins. J Exp Bot. doi:10.1093/jxb/erq352
Wang X, Meyers D, Yan Y, Baum T, Smant G et al (1999) In planta localisation of a β-1,4-Endoglucanase secreted by Heterodera glycines. Mol Plant Microbe Interact 12:64–67
Wang X, Mitchum MG, Gao B, Li C, Diab H et al (2005) A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol Plant Pathol 6:187–191
Wang X, Li H, Hu Y, Fu P, Xu J (2007) Molecular cloning and analysis of a new venom allergen-like protein gene from the root-knot nematode Meloidogyne incognita. Exp Parasitol 117:133–140
Wang J, Lee C, Replogle A, Joshi S, Korkin D, Hussey RS, Baum TJ, Davies RL, Wang X, Mitchum M (2010). Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytologist 187:1003–1017
Weerasinghe R, Bird D, Allen N (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proc Natl Acad Sci U S A 102:3147–3152
Wienkoop S, Saalbach G (2003) Proteome Analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Phys 131:1080–1090
Williamson AL, Brindley PJ, Knox DP, Hotez PJ, Loukas A (2003) Digestive proteases of blood-feeding nematodes. Trends Parasitol 19:417–423
Zahler AM (2005) Alternative splicing in C. elegans. Wormbook, The C. elegans Research Community, www.wormbook.org
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With a kind thought to our colleague and friend Qin Ling and his major contribution in the field of nematode effectors.
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Rosso, MN., Grenier, E. (2011). Other Nematode Effectors and Evolutionary Constraints. In: Jones, J., Gheysen, G., Fenoll, C. (eds) Genomics and Molecular Genetics of Plant-Nematode Interactions. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0434-3_14
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