Identification and Characterisation of a Hyper-Variable Apoplastic Effector Gene Family of the Potato Cyst Nematodes

PLoS Pathogens

Volumn 10, Issue 9, 2014, Pages

  Eves van den Akker, Sebastian ^a,b   Lilley, Catherine J ^a   Jones, John T ^b   Urwin, Peter E ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; APOPLAST; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; COPY NUMBER VARIATION; FLUORESCENCE IN SITU HYBRIDIZATION; GLOBODERA; IMMUNOCHEMISTRY; MOLECULAR CLONING; NONHUMAN; PARASITISM; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SECRETORY CELL; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; BIOLOGY; CELL WALL; CHEMISTRY; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; HOST PARASITE INTERACTION; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; LIFE CYCLE STAGE; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; NEMATODIASIS; PARASITOLOGY; PLANT CELL; PLANT DISEASE; PLANT ROOT; POTATO; SEQUENCE HOMOLOGY; TYLENCHOIDEA;

NEMATODA; SOLANUM TUBEROSUM;

HELMINTH DNA; HELMINTH PROTEIN;

AMINO ACID SEQUENCE; ANIMALS; CELL WALL; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; DNA COPY NUMBER VARIATIONS; DNA, HELMINTH; HELMINTH PROTEINS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOST-PARASITE INTERACTIONS; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; LIFE CYCLE STAGES; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PLANT CELLS; PLANT DISEASES; PLANT ROOTS; SECERNENTEA INFECTIONS; SEQUENCE HOMOLOGY, AMINO ACID; SOLANUM TUBEROSUM; TYLENCHOIDEA;

EID: 84907573595     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004391     Document Type: Article

References (64)

1. Trudgill DL, (1997) Parthenogenetic root-knot nematodes (Meloidogyne spp); How can these biotrophic endoparasites have such an enormous host range? Plant Pathology 46: 26–32.
2. Nicol JM, Turner SJ, Coyne DL, den Nijs L, Hockland S, et al. (2011) Current Nematode Threats to World Agriculture. In: Jones J, Gheysen G, Fenoll C, editors. Genomics and Molecular Genetics of Plant-Nematode Interactions. pp. 21–43.
3. 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.
4. Wyss U, (1992) Observations on the feeding behaviour of Heterodera schachtii throughout development including events during moulting. Fundamental and Applied Nematology 15: 75–89.
5. Haegeman A, Mantelin S, Jones JT, Gheysen G, (2012) Functional roles of effectors of plant-parasitic nematodes. Gene 492: 19–31.
6. Hewezi T, Baum TJ, (2013) Manipulation of plant cells by cyst and root-knot nematode effectors. Molecular Plant-Microbe Interactions 26: 9–16.
7. Lilley CJ, Urwin PE, Atkinson HJ, McPherson MJ, (1997) Characterization of cDNAs encoding serine proteinases from the soybean cyst nematode Heterodera glycines. Molecular and Biochemical Parasitology 89: 195–207.
8. Gheysen G, Fenoll C, (2002) Gene expression in nematode feeding sites. Annual Review of Phytopathology 40: 191–219.
9. Wang XH, Mitchum MG, Gao BL, Li CY, Diab H, et al. (2005) A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Molecular Plant Pathology 6: 187–191.
10. Replogle A, Wang J, Bleckmann A, Hussey RS, Baum TJ, et al. (2011) Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. The Plant Journal 65: 430–440.
11. Semblat J-P, Rosso M-N, 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. Molecular Plant-Microbe Interactions 14: 72–79.
12. Vieira P, Danchin EGJ, Neveu C, Crozat C, Jaubert S, et al. (2011) The plant apoplasm is an important recipient compartment for nematode secreted proteins. Journal of Experimental Botany 62: 1241–1253.
13. Rosso M-N, Vieira P, de Almeida-Engler J, Castagnone-Sereno P, (2011) Proteins secreted by root-knot nematodes accumulate in the extracellular compartment during root infection. Plant Signal Behav 6: 1232–1234.
14. Endo BY, (1978) Feeding plug formation in soybean roots infected with the soybean cyst nematode. Phytopathology 68: 1022–1031.
15. Sobczak M, Golinowski WA, Grundler FMW, (1999) Ultrastructure of feeding plugs and feeding tubes formed by Heterodera schachtii. Nematology 1: 363–374.
16. Gao BL, Allen R, Maier T, Davis EL, Baum TJ, et al. (2003) The parasitome of the phytonematode Heterodera glycines. Molecular Plant-Microbe Interactions 16: 720–726.
17. 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. Molecular Plant-Microbe Interactions 16: 376–381.
18. Perry RN, (1996) Chemoreception in plant parasitic nematodes. Annual Review of Phytopathology 34: 181–199.
19. Jones JT, Perry RN, Johnston MRL, (1994) Changes in the ultrastructure of the amphids of the potato cyst-nematode, Globodera rostochiensis, during development and infection. Fundamental and Applied Nematology 17: 369–382.
20. Tomalova I, Iachia C, Mulet K, Castagnone-Sereno P, (2012) The map-1 gene family in root-knot nematodes, Meloidogyne spp.: a set of taxonomically restricted genes specific to clonal species. Plos One 7: e38656.
21. Jones J, Reavy B, Smant G, Prior A, (2004) Glutathione peroxidases of the potato cyst nematode Globodera Rostochiensis. Gene 324: 47–54.
22. Cotton JA, Lilley CJ, Jones LM, Kikuchi T, Reid AJ, et al. (2014) The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome Biology 15: R43.
23. Wubben MJ, Callahan FE, Scheffler BS, (2010) Transcript analysis of parasitic females of the sedentary semi-endoparasitic nematode Rotylenchulus reniformis. Molecular and Biochemical Parasitology 172: 31–40.
24. Jacob J, Mitreva M, Vanholme B, Gheysen G, (2008) Exploring the transcriptome of the burrowing nematode Radopholus similis. Molecular Genetics and Genomics 280: 1–17.
25. 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. Nature Biotechnology 26: 909–915.
26. Opperman CH, Bird DM, Williamson VM, Rokhsar DS, Burke M, et al. (2008) Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences 105: 14802–14807.
27. Castagnone-Sereno P, Semblat J-P, Castagnone C, (2009) Modular architecture and evolution of the map-1 gene family in the root-knot nematode Meloidogyne incognita. Molecular Genetics and Genomics 282: 547–554.
28. Rutter WB, Hewezi T, Maier TR, Mitchum MG, Davis EL, et al. (2014) Members of the Meloidogyne Avirulence protein family contain multiple plant ligand-like motifs. Phytopathology 104: 879–885.
29. Doyle EL, Stoddard BL, Voytas DF, Bogdanove AJ, (2013) TAL effectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends in Cell Biology 23: 390–398.
30. Stam R, Howden AJ, Delgado-Cerezo M, Amaro TM, Motion GB, et al. (2013) Characterization of cell death inducing Phytophthora capsici CRN effectors suggests diverse activities in the host nucleus. Frontiers in plant science 4: 387.
31. Stam R, Jupe J, Howden AJ, Morris JA, Boevink PC, et al. (2013) Identification and characterisation CRN Effectors in Phytophthora capsici shows modularity and functional diversity. PLoS ONE 8: e59517.
32. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450: 115–118.
33. Scott JA, Collins FH, Feyereisen R, (1994) Diversity of cytochrome-p450 genes in the mosquito, Anopheles albimanus. Biochemical and biophysical research communications 205: 1452–1459.
34. Ranson H, Nikou D, Hutchinson M, Wang X, Roth CW, et al. (2002) Molecular analysis of multiple cytochrome P450 genes from the malaria vector, Anopheles gambiae. Insect Molecular Biology 11: 409–418.
35. Wondji CS, Irving H, Morgan J, Lobo NF, Collins FH, et al. (2009) Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Research 19: 452–459.
36. Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, et al. (2008) Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Southern Benin and Nigeria. Bmc Genomics 9: 538.
37. Barone A, Ritter E, Schachtschabel U, Debener T, Salamini F, et al. (1990) Localization by restriction-fragment-length-polymorphism mapping in potato of a major dominant gene conferring resistance to the potato cyst nematode Globodera rostochiensis. Molecular & General Genetics 224: 177–182.
38. Sasagawa Y, Nikaido I, Hayashi T, Danno H, Uno KD, et al. (2013) Quartz-Seq: a highly reproducible and sensitive single-cell RNA sequencing method, reveals non-genetic gene-expression heterogeneity. Genome Biology 14: R31.
39. Alenda C, Gallot-Legrand A, Fouville D, Grenier E, (2013) Sequence polymorphism of nematode effectors highlights molecular differences among the subspecies of the tobacco cyst nematode complex. Physiological and Molecular Plant Pathology 84: 107–114.
40. Plantard O, Picard D, Valette S, Scurrah M, Grenier E, et al. (2008) Origin and genetic diversity of Western European populations of the potato cyst nematode (Globodera pallida) inferred from mitochondrial sequences and microsatellite loci. Molecular Ecology 17: 2208–2218.
41. Thiery M, Fouville D, Mugniery D, (1997) Intra- and interspecific variability in Globodera, parasites of Solanaceous plants, revealed by random amplified polymorphic DNA (RAPD) and correlation with biological features. Fundamental and Applied Nematology 20: 495–504.
42. Blok VC, Malloch G, Harrower B, Phillips MS, Vrain TC, (1998) Intraspecific variation in ribosomal DNA in populations of the potato cyst nematode Globodera pallida. Journal of Nematology 30: 262–274.
43. Lilley CJ, Bakhetia M, Charlton WL, Urwin PE, (2007) Recent progress in the development of RNA interference for plant parasitic nematodes. Molecular Plant Pathology 8: 701–711.
44. Lilley C, Davies L, Urwin P, (2012) RNA interference in plant parasitic nematodes: a summary of the current status. Parasitology 139: 630–640.
45. Wubben MJ, Callahan FE, Triplett BA, Jenkins JN, (2009) Phenotypic and molecular evaluation of cotton hairy roots as a model system for studying nematode resistance. Plant Cell Reports 28: 1399–1409.
46. Triplett BA, Moss SC, Bland JM, Dowd MK, (2008) Induction of hairy root cultures from Gossypium hirsutum and Gossypium barbadense to produce gossypol and related compounds. In Vitro Cellular & Developmental Biology-Plant 44: 508–517.
47. Dalzell JJ, McVeigh P, Warnock ND, Mitreva M, Bird DM, et al. (2011) RNAi effector diversity in nematodes. PLoS neglected tropical diseases 5: e1176.
48. Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, et al. (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14: 946–961.
49. Holterman M, Karssen G, van den Elsen S, van Megen H, Bakker J, et al. (2009) Small Subunit rDNA-based phylogeny of the Tylenchida sheds light on relationships among some high-impact plant-parasitic nematodes and the evolution of plant feeding. Phytopathology 99: 227–235.
50. Barrett LW, Fletcher S, Wilton SD, (2012) Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cellular and Molecular Life Sciences 69: 3613–3634.
51. Zhao W, Blagev D, Pollack JL, Erle DJ, (2011) Toward a systematic understanding of mRNA 3′ untranslated regions. Proceedings of the American Thoracic Society 8: 163–166.
52. Suarez Z, Moss CS, Inserra RN, (1985) Anatomical changes induced by Punctodera chalcoensis in corn roots. Journal of Nematology 17: 242–244.
53. Cohn E, Mordechai M, (1982) Biology and host parasite relations of a species of Meloidoderita nematoda criconematoidea. Revue de Nematologie 5: 247–256.
54. Vovlas N, Inserra RN, (1986) Morphometrics, illustration, and histopathology of Sphaeronema rumicis on cottonwood in Utah. Journal of Nematology 18: 239–246.
55. Jones MGK, Payne HL, (1977) Structure of syncytia induced by phytoparasitic nematode Nacobbus aberrans in tomato roots, and possible role of plasmodesmata in their nutrition. Journal of Cell Science 23: 299–313.
56. Eves-van den Akker S, Lilley C, Danchin E, Rancurel C, Cock P, et al. (2014) The transcriptome of Nacobbus aberrans reveals insights into the evolution of sedentary endoparasitism in plant-parasitic nematodes. Genome Biology and Evolution evu171.
57. Triant DA, Whitehead A, (2009) Simultaneous extraction of high-quality RNA and DNA from small tissue samples. Journal of Heredity 100: 246–250.
58. de Boer JM, Yan Y, Smant G, Davis EL, Baum TJ, (1998) In situ hybridization to messenger RNA in Heterodera glycines. J Nematol 30: 309–312.
59. Davies LJ, Lilley CJ, Knox JP, Urwin PE, (2012) Syncytia formed by adult female Heterodera schachtii in Arabidopsis thaliana roots have a distinct cell wall molecular architecture. New Phytologist 196: 238–246.
60. Hopp TP, Woods KR, (1981) Prediction of protein antigenic determinants from amino acid sequences. Proceedings of the National Academy of Sciences 78: 3824–3828.
61. Wesley SV, Helliwell CA, Smith NA, Wang M, Rouse DT, et al. (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. The Plant Journal 27: 581–590.
62. Gleave AP, (1992) A versatile binary vector system with a T-DNA organizational-structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology 20: 1203–1207.
63. Petersen TN, Brunak S, von Heijne G, Nielsen H, (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8: 785–786.
64. Bird AF, Bird J (1991) The structure of nematodes. San Diego (California): Academic Press.