Heterozygote deficits in cyst plant-parasitic nematodes: Possible causes and consequences

Molecular Ecology

Volumn 24, Issue 8, 2015, Pages 1654-1664

  Montarry, Josselin ^a   Jan, Pierre Loup ^a   Gracianne, Cecile ^a   Overall, Andrew D J ^b   Bardou Valette, Sylvie ^a   Olivier, Eric ^a   Fournet, Sylvain ^a   Grenier, Eric ^a   Petit, Eric J ^c  

^a Universite Rennes 1   (France)

^b UNIVERSITY OF BRIGHTON   (United Kingdom)

^c Ecology and Ecosystem Health   (France)

Author keywords

consanguinity; heterozygote deficit; microsatellite; nematode; null allele; Wahlund effect

Indexed keywords

BETA VULGARIS SUBSP. VULGARIS; GLOBODERA PALLIDA; HETERODERA SCHACHTII; NEMATODA; NICOTIANA TABACUM; SOLANUM TUBEROSUM;

MICROSATELLITE DNA;

ALLELE; ANIMAL; BEET; GENE FREQUENCY; GENETIC VARIABILITY; GENETICS; GENOTYPE; HETEROZYGOTE; INBREEDING; PARASITOLOGY; POPULATION GENETICS; POTATO; STATISTICAL MODEL; TOBACCO; TYLENCHOIDEA;

ALLELES; ANIMALS; BETA VULGARIS; GENE FREQUENCY; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPE; HETEROZYGOTE; INBREEDING; LIKELIHOOD FUNCTIONS; MICROSATELLITE REPEATS; SOLANUM TUBEROSUM; TOBACCO; TYLENCHOIDEA;

EID: 84926524937     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13142     Document Type: Article

References (62)

1. Adams HH, Osborne WW, Webber AJ, (1982) Effect of temperature on development and reproduction of Globodera solanacearum. Nematropica, 12, 305-311.
2. Alenda C, Montarry J, Grenier E, (2014) Human influence on the dispersal and genetic structure of French Globodera tabacum populations. Infection, Genetics and Evolution, 27, 309-317.
3. Alexandrino J, Baird SJE, Lawson L, et al,. (2005) Strong selection against hybrids at a hybrid zone in the Ensatina ring species complex and its evolutionary implications. Evolution, 59, 1334-1347.
4. Balloux F, (2001) easypop (Version 1.7): a computer program for population genetics simulations. Journal of Heredity, 92, 301-302.
5. Beaumont M, Barratt EM, Gottelli D, et al,. (2001) Genetic diversity and introgression in the Scottish wildcat. Molecular Ecology, 10, 319-336.
6. Belkhir K, Borsa P, Chikhi L, et al,. (1996 -2004) genetix 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France).
7. Boucher AC, Mimee B, Montarry J, et al,. (2013) Genetic diversity of the golden potato cyst nematode Globodera rostochiensis and determination of the origin of populations in Quebec, Canada. Molecular Phylogenetics and Evolution, 69, 75-82.
8. Brookfield JFY, (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology, 5, 453-455.
9. Brouat C, Tatard C, Machin A, et al,. (2011) Comparative population genetics of a parasitic nematode and its host community: the trichostrongylid Neoheligmonella granjoni and Mastomys rodents in southeastern Senegal. International Journal for Parasitology, 41, 1301-1309.
10. Callen DF, Thompson AD, Shen Y, et al,. (1993) Incidence and origin of "null" alleles in the (AC)n microsatellite markers. American Journal of Human Genetics, 52, 922-927.
11. Castric V, Bernatchez L, Belkhir K, Bonhomme F, (2002) Heterozygote deficiencies in small lacustrine populations of brook charr Salvelinus fontinalis Mitchill (Pisces, Salmonidae): a test of alternative hypotheses. Heredity, 89, 27-35.
12. Chapuis MP, Estoup A, (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24, 621-631.
13. Chybicki IJ, Burczyk J, (2009) Simultaneous estimation of null alleles and inbreeding coefficients. Journal of Heredity, 100, 106-113.
14. Cooke DA, (1992) Beet cyst nematode (Heterodera schachtii Schmidt) and its control on sugar beet. In: Plant Diseases of International Importance, IV. Diseases of Sugar, Foret and Plantation Crops (eds, Mukhopadayay AN, Kumar J, Singh US, Chaube HS,), pp. 135-183. Prenctice Hall, Upper Saddle River, New Jersey.
15. Cornell SJ, Isham VS, Smith G, Grenfell BT, (2003) Spatial parasite transmission, drug resistance, and the spread of rare genes. Proceedings of the National Academy of Sciences, USA, 100, 7401-7405.
16. Cotton JA, Lilley CJ, Jones LM, et al,. (2014) The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by cyst nematode. Genome Biology, 15, R43.
17. Dharmarajan G, Beasley JC, Rhodes OE Jr, (2010) Spatial and temporal factors affecting parasite genotypes encountered by hosts: empirical data from American dog ticks (Dermacentor variabilis) parasiting raccoons (Procyon lotor). International Journal of Parasitology, 40, 787-795.
18. Dharmarajan G, Beasley JC, Rhodes OE Jr, (2011) Heterozygote deficiencies in parasite populations: an evaluation of interrelated hypotheses in the raccoon tick, Ixodes texanus. Heredity, 106, 253-260.
19. FitzSimmons NN, Moritz C, Moore SS, (1995) Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Molecular Biology and Evolution, 12, 432-440.
20. Flor HH, (1942) Inheritance of pathogenicity in Melampsora lini. Phytopathology, 32, 653-669.
21. Flor HH, (1956) The complementary genic systems in flax and flax rust. Advance in Genetics, 8, 29-54.
22. Flor HH, (1971) Current status of the gene-for-gene concept. Annual Review of Phytopathology, 9, 275-296.
23. Fournet S, Kerlan MC, Renault L, et al,. (2013) Selection of nematodes by resistant plants has implications for local adaptation and cross-virulence. Plant Pathology, 62, 184-193.
24. Fredholm M, Wintero AK, (1995) Variation of short tandem repeats within and between species belonging to the Canidae family. Mammal Genome, 6, 11-18.
25. Gilabert A, Wasmuth JD, (2013) Unravelling parasitic nematode natural history using population genetics. Trends in Parasitology, 29, 438-448.
26. Goudet J, Perrin N, Waser P, (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Molecular Ecology, 11, 1103-1114.
27. Grenier E, Fournet S, Petit E, Anthoine G, (2010) A cyst nematode 'species factory' called the Andes. Nematology, 12, 163-169.
28. Grillo V, Jackson F, Cabaret J, Gilleard JS, (2007) Population genetic analysis of the ovine parasitic nematode Teladorsagia circumcincta and evidence for a cryptic species. International Journal for Parasitology, 37, 435-447.
29. Grundler F, Betka M, Wyss U, (1991) Influence of changes in the nurse cell system (syncytium) on sex determination and development of the cyst nematode Heterodera schachtii: total amounts of proteins and amino acids. Phytopathology, 81, 70-74.
30. Guzinski J, Bull CM, Donnellan SC, Gardner MG, (2009) Molecular genetic data provide support for a model of transmission dynamics in an Australian reptile tick, Bothriocroton hydrosauri. Molecular Ecology, 18, 227-234.
31. Holleley CE, Geerts PG, (2009) multiplex manager 1.0: a cross-platform computer program that plans and optimizes multiplex PCR. BioTechniques, 46, 511-517.
32. Janssen R, Bakker J, Gommers FJ, (1991) Mendelian proof for a gene-for-gene relationship between virulence of Globodera rostochiensis and the H1 resistance gene in Solanum tuberosum ssp. andigena CPC 1673. Revue de Nématologie, 14, 207-211.
33. Johnson CS, (1998) Tobacco. In: Plant Nematode Interactions (eds, Barker KR, Pederson GA, Windham GL,), pp. 487-522. American Society of Agronomists, Madison, Wisconsin.
34. Jones JDG, Dangl JL, (2006) The plant immune system. Nature, 444, 323-329.
35. Jones MGK, Northcote DH, (1972) Nematode-induced syncytium-a multinucleate transfer cell. Journal of Cell Science, 10, 789-809.
36. Langella O, (2000) populations 1·2: population genetic software, individuals or population distance, phylogenetic trees. http://bioinformatics.org/~tryphon/populations/
37. Malausa T, Gilles A, Meglécz E, et al,. (2011) High throughput microsatellites isolation with 454 GS-FLX Titanium pyrosequencing. Molecular Ecology Resources, 11, 638-644.
38. McDonald BA, Linde C, (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349-379.
39. Meglécz E, Costedoat C, Dubut V, et al,. (2010) QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics, 26, 403-404.
40. Nei M, (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583-590.
41. Overall ADJ, Nichols RA, (2001) A method for distinguishing consanguinity and population substructure using multilocus genotype data. Molecular Biology and Evolution, 18, 2048-2056.
42. Paxton RJ, Thoren PA, Tengö J, et al,. (1996) Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Molecular Ecology, 5, 511-519.
43. Picard D, Plantard O, Scurrah M, Mugniéry D, (2004) Inbreeding and population structure of the potato cyst nematode (Globodera pallida) in its native area (Peru). Molecular Ecology, 13, 2899-2908.
44. Plantard O, Porte C, (2004) Population genetic structure of the sugar beet cyst nematode Heterodera schachtii: a gonochoristic and amphimictic species with highly inbred but weakly differentiated populations. Molecular Ecology, 13, 33-41.
45. Pompanon F, Bonin A, Bellemain E, Taberlet P, (2005) Genotyping errors: causes, consequences and solutions. Nature Reviews Genetics, 6, 847-859.
46. R Development Core Team (2012) R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria.
47. Raski DJ, (1950) The life history and morphology of the sugar beet nematode, Heterodera schachtii Schmidt. Phytopathology, 40, 135-151.
48. Rougeron V, De Meeûs T, Hide M, et al,. (2009) Extreme inbreeding in Leishmania braziliensis. Proceedings of the National Academy of Sciences, USA, 106, 10224-10229.
49. Sasser JN, Freckman DW, (1987) A world perspective on Nematology: the role of the society. In: Vistas on Nematology (eds, Veech JA, Dickson DW,), pp. 7-14. Society of Nematologists, Hyattsville, Maryland.
50. Selkoe KA, Toonen RJ, (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters, 9, 615-629.
51. Silvestre A, Sauve C, Cortet J, Cabaret J, (2009) Contrasting genetic structures of two parasitic nematodes, determined on the basis of neutral microsatellite markers and selected anthelmintic resistance markers. Molecular Ecology, 18, 5086-5100.
52. Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JDG, (1995) Molecular genetics of plant disease resistance. Science, 268, 661-667.
53. Taberlet P, Griffin S, Goossens B, et al,. (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Research, 24, 3189-3194.
54. Thiele EA, Sorensen RE, Gazzinelli A, Minchella DJ, (2008) Genetic diversity and population structuring of Schistosoma mansoni in a Brazilian village. International Journal of Parasitology, 38, 389-399.
55. Thiéry M, Mugniéry D, (1996) Interspecific rDNA restriction fragment length polymorphisms in Globodera species, parasites of solanaceous plants. Fundamental and Applied Nematology, 19, 471-479.
56. Toth G, Gaspari Z, Jurka J, (2000) Microsatellites in different eukaryotic genomes: survey and analysis. Genome Research, 10, 967-981.
57. Trudgill DL, (1967) The effect of environment on the sex determination in Heterodera rostochiensis. Nematologica, 13, 263-272.
58. Vanderplank JE, (1963) Plant Diseases: Epidemics and Control. Academic Press, New York, New York.
59. Vanderplank JE, (1968) Disease Resistance in Plants. Academic Press, New York, New York.
60. Wahlund S, (1928) Zusammensetzung von Population und Korrelationserscheinung vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas, 11, 65-106.
61. Wallace HR, (1968) The dynamics of nematode movement. Annual Review of Phytopathology, 6, 91-114.
62. Waples RS, Gaggiotti O, (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Molecular Ecology, 15, 1419-1439.