Sequence polymorphism of nematode effectors highlights molecular differences among the subspecies of the tobacco cyst nematode complex

Physiological and Molecular Plant Pathology

Volumn 84, Issue 1, 2013, Pages 107-114

  Alenda, Charline ^a   Gallot Legrand, Aurore ^a   Fouville, Didier ^a   Grenier, Eric ^a  

^a Universite Rennes 1   (France)

Author keywords

Clavata like ESR; Diagnostic; Expansin; Globodera tabacum; Pectate lyase; Species complex

Indexed keywords

EID: 84884374756     PISSN: 08855765     EISSN: 10961178     Source Type: Journal    
DOI: 10.1016/j.pmpp.2013.08.004     Document Type: Article

References (46)

1. La Mondia J.A. Shade tobacco yield loss and Globodera tabacum tabacum population changes in relation to initial nematode density. JNematol 1995, 27:114-119.
2. Lownsberry B.F., Lownsberry J.W. Heterodera tabacum new species, a parasite of Solanaceaous plants in Connecticut. Proc Helminthol Soc Wash 1954, 21:42-47.
3. Stone A.R., Platt H.M., Khalil L.F. Three approaches to the status of a species complex, with a revision of some species of Globodera. Concepts in nematode systematics 1983, 221-223. Academic Press, London. A.R. Stone, H.M. Platt, L.F. Khalil (Eds.).
4. Miller L.I., Gray B.J. Horsenettle cyst nematode, Heterodera virginiae n.sp., a parasite of solanaceous plants. Nematologica 1968, 14:535-543.
5. Miller L.I., Gray B.J. Heterodera solanacearum n. sp., a parasite of solanaceaous plants. Nematologica 1972, 18:404-413.
6. Motta M., Eisenback J. Morphology of second-stages juveniles and males of Globodera tabacum tabacum, G. t. virginiae, and G.t. solanacearum (Nemata: Heteroderinae). JNematol 1993, 25:27-33.
7. Mugniéry D., Bossis M., Pierre J.S. Hybridations entre Globodera rostochiensis (Wollenweber), G.pallida (Stone), G.virginiae (Miller and Gray), G.solanacearum (Miller and Gray), et G. "mexicana" (Campos-Vela). Description et devenir des hybrides. Fundam Appl Nematol 1992, 15:375-382.
8. Herrero S., Rufty R.C., Barker K.R. Evaluation of tobacco germ plasm for resistance to the tobacco cyst nematode, Globodera tabacum solanacearum. Plant Dis 1996, 80:61-65.
9. La Mondia J.A. Genetics of tobacco resistance to Globodera tabacum tabacum. Plant Dis 1991, 75:453-454.
10. CAB International Globodera tabacum. Distribution maps of plant diseases 2004, Map. 929.
11. Subbotin S.A., Cid Del Prado Vera I., Mundo-Ocampo M., Baldwin J.G. Identification, phylogeny and phylogeography of circumfenestrate cyst nematodes (Nematoda: Heteroderidae) as inferred from analysis of ITS-rDNA. Nematology 2011, 13:805-824.
12. Thiéry M., Fouville D., Mugniéry D. Intra and interspecific variability in Globodera, parasites of Solanaceous plants, revealed by random amplified polymorphic DNA (RAPD) and correlation with biological features. Fundam Appl Nematol 1997, 20:495-504.
13. Marché L., Valette S., Grenier E., Mugniéry D. Intra-species DNA polymorphism in the tobacco cyst-nematode complex (Globodera tabacum) using AFLP. Genome 2001, 44:941-946.
14. 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. JNematol 2000, 32:154-165.
15. Stare B.G., Fouville D., Sirca S., Gallot A., Urek G., Grenier E. Molecular variability and evolution of the pectate lyase (pel-2) parasitism gene in cyst nematodes parasitizing different solanaceous plants. JMol Evol 2011, 72:169-181.
16. Yu H., Chronis D., Lu S.W., Wang X.H. Chorismate mutase: an alternatively spliced parasitism gene and a diagnostic marker for three important Globodera nematode species. Eur J Plant Pathol 2011, 129:89-102.
17. Haegeman A., Mantelin S., Jones J.T., Gheysen G. Functional roles of effectors of plant-parasitic nematodes. Gene 2012, 492:19-31.
18. Rehman S., Butterbach P., Popeijus H., Overmars H., Davis E.L., Jones J.T., et al. Identification and characterization of the most abundant cellulases in stylet secretions from Globodera rostochiensis. Phytopathology 2009, 99:194-202.
19. Kudla U., Qin L., Milac A., Kielak A., Maissen C., Overmars H., et al. Origin, distribution and 3D-modeling of Gr-EXPB1, an expansin from the potato cyst nematode Globodera rostochiensis. FEBS 2005, 579:2451-2457.
20. Lu S.W., Chen S., Wang J., Yu H., Chronis D., Mitchum M.G., 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.
21. De Boer J.M., McDermott J.P., Davis E.L., Hussey R.S., Popeijus H., Smant G., et al. Cloning of a putative pectate lyase gene expressed in the subventral esophageal glands of Heterodera glycines. JNematol 2002, 34:9-11.
22. Gao B.L., 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. JNematol 2002, 34:12-15.
23. Wang X.H., Mitchum M.G., Gao B.L., Li C.Y., Diab H., Baum T.J., et al. Aparasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol Plant Pathol 2005, 6:187-191.
24. Vanholme B., Van Thuyne W., Vanhouteghem K.A., 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.
25. Wang J.Y., Replogle A., Hussey R., Baum T., Wang X.H., Davis E.L., 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.
26. Mitchum M.G., Wang X.H., Wang J.Y., Davis E.L. Role of nematode peptides and other small molecules in plant parasitism. Annu Rev Phytopathol 2012, 50:175-195.
27. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
28. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
29. Posada D. ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Res 2006, 34:W700-W703.
30. Phillips M.S., Blok V.C., Ploeg A., Harrower B.E. Studies on an artificially fragmented population of potato cyst nematode Globodera pallida. Nematologica 1998, 44:655-666.
31. Kikuchi T., Hongmei L., 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.
32. Stare B.G., Lamovsek J., Sirca S., Urek G. Assessment of sequence variability in putative parasitism factor, expansin (expB2) from diverse populations of potato cyst nematode Globodera rostochiensis. Physiol Mol Plant Pathol 2012, 79:49-54.
33. Abad P., Gouzy J., Aury J.M., Castagnone-Sereno P., Danchin E.G.J., Deleury E., et al. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 2008, 26:909-915.
34. Danchin E.G.J., Rosso M.N., Vieira P., de Almeida-Engler J., Coutinho P.M., Henrissat B., et al. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci USA 2010, 107:17651-17656.
35. Wang J.Y., Lee C., Replogle A., Joshi S., Korkin D., Hussey R., 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.
36. Leache A.D. Species trees for spiny lizards (Genus Sceloporus): Identifying points of concordance and conflict between nuclear and mitochondrial data. Mol Phylogen Evol 2010, 54:162-171.
37. Camargo A., Avila L.J., Morando M., Sites J.W. Accuracy and precision of species trees: effects of locus, individual, and base pair sampling on inference of species trees in lizards of the Liolaemus darwinii group (Squamata, Liolaemidae). Syst Biol 2012, 61:272-288.
38. Lee J.Y., Joseph L., Edwards S.V. Aspecies tree for the Australo-Papuan fairywrens and allies (Aves: Maluridae). Syst Biol 2012, 61:253-271.
39. Steppan S.J., Adkins R.M., Spinks P.Q., Hale C. Multigene phylogeny of the Old World mice, Murinae, reveals distinct geographic lineages and the declining utility of mitochondrial genes compared to nuclear genes. Mol Phylogen Evol 2005, 37:370-388.
40. Uchiyama H., Chen K., Wildman S.G. Polypeptide composition of fraction I protein as an aid in the study of plant evolution. Stadler Symp 1977, 9:83-99.
41. Picard D., Sempere T., Plantard O. Direction and timing of uplift propagation in the Peruvian Andes deduced from molecular phylogenetics of highland biotaxa. Earth Planet Sci Lett 2008, 271:326-336.
42. Bekal S., Niblack T.L., Lambert K.N. Achorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence. Mol Plant Microbe Interact 2003, 16:439-446.
43. Sacco M.A., Koropacka K., Grenier E., Jaubert M.J., Blanchard A., Goverse A., et al. The cyst nematode SPRYSEC protein RBP-1 Elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathog 2009, 5:e1000564.
44. Lozano-Torres J.L., Wilbers R.H.P., Gawronski P., Boshoven J.C., Finkers-Tomczak A., Cordewener J.H.G., et al. Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. Proc Natl Acad Sci USA 2012, 109:10119-10124.
45. Powers T. Nematode molecular diagnostics: from bands to barcodes. Annu Rev Phytopathol 2004, 42:367-383.
46. Powers T.O., Harris T.S. Apolymerase chain reaction method for identification of five major Meloidogyne species. JNematol 1993, 25:1-6.