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

Josselin Montarry, Jan Pierre-Loup, Cecile Gracianne, Andrew Overall, Sylvie Bardou-Valette, Eric Olivier, Sylvain Fournet, Eric Grenier, Eric J. Petit

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Deviations of genotypic frequencies from Hardy–Weinberg equilibrium (HWE) expectations could reveal important aspects of the biology of populations. Deviations from HWE due to heterozygote deficits have been recorded for three plant-parasitic nematode species. However, it has never been determined whether the observed deficits were due (i) to the presence of null alleles, (ii) to a high level of consanguinity and/or (iii) to a Wahlund effect. The aim of the present work was, while taking into the possible confounding effect of null alleles, to disentangle consanguinity and Wahlund effect in natural populations of those three economically important cyst nematodes using microsatellite markers:Globodera pallida,G.tabacumandHeterodera schachtii, pests of potato, tobacco and sugar beet, respectively. The results show a consistent pattern of heterozygote deficiency in the three nematode species sampled at the spatial scale of the host plant. We demonstrate that the prevalence of null alleles is weak and that heterozygote deficits do not have a single origin. Our results suggested that it is restricted dispersal that leads to heterozygote deficits through both consanguinity and substructure, which effects can be linked to soil movement, cyst density, and the number of generations per year. We discuss potential implications for the durability of plant resistances that are used to protect crops against parasites in which mating between relatives occur. While consanguineous mating leads to homozygosity at all loci, including loci governing avirulence/virulence, which favours the expression of virulence when recessive, the Wahlund effect is expected to have no particular effect on the adaptation of nematodes to resistances.
Original languageEnglish
Pages (from-to)1654-1677
Number of pages24
JournalMolecular Ecology
Volume24
Issue number8
DOIs
Publication statusPublished - 3 Apr 2015

Fingerprint

plant parasitic nematodes
null alleles
heterozygosity
virulence
Nematoda
Globodera pallida
soil movement
loci
cyst nematodes
durability
homozygosity
sugar beet
tobacco
host plants
pests
potatoes
microsatellite repeats
parasites
Biological Sciences
crops

Keywords

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

Cite this

Montarry, J., Pierre-Loup, J., Gracianne, C., Overall, A., Bardou-Valette, S., Olivier, E., ... Petit, E. J. (2015). Heterozygote deficits in cyst plant-parasitic nematodes: possible causes and consequences. Molecular Ecology, 24(8), 1654-1677. https://doi.org/10.1111/mec.13142
Montarry, Josselin ; Pierre-Loup, Jan ; Gracianne, Cecile ; Overall, Andrew ; Bardou-Valette, Sylvie ; Olivier, Eric ; Fournet, Sylvain ; Grenier, Eric ; Petit, Eric J. / Heterozygote deficits in cyst plant-parasitic nematodes: possible causes and consequences. In: Molecular Ecology. 2015 ; Vol. 24, No. 8. pp. 1654-1677.
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Montarry, J, Pierre-Loup, J, Gracianne, C, Overall, A, Bardou-Valette, S, Olivier, E, Fournet, S, Grenier, E & Petit, EJ 2015, 'Heterozygote deficits in cyst plant-parasitic nematodes: possible causes and consequences', Molecular Ecology, vol. 24, no. 8, pp. 1654-1677. https://doi.org/10.1111/mec.13142

Heterozygote deficits in cyst plant-parasitic nematodes: possible causes and consequences. / Montarry, Josselin; Pierre-Loup, Jan; Gracianne, Cecile; Overall, Andrew; Bardou-Valette, Sylvie; Olivier, Eric; Fournet, Sylvain; Grenier, Eric; Petit, Eric J.

In: Molecular Ecology, Vol. 24, No. 8, 03.04.2015, p. 1654-1677.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Heterozygote deficits in cyst plant-parasitic nematodes: possible causes and consequences

AU - Montarry, Josselin

AU - Pierre-Loup, Jan

AU - Gracianne, Cecile

AU - Overall, Andrew

AU - Bardou-Valette, Sylvie

AU - Olivier, Eric

AU - Fournet, Sylvain

AU - Grenier, Eric

AU - Petit, Eric J.

PY - 2015/4/3

Y1 - 2015/4/3

N2 - Deviations of genotypic frequencies from Hardy–Weinberg equilibrium (HWE) expectations could reveal important aspects of the biology of populations. Deviations from HWE due to heterozygote deficits have been recorded for three plant-parasitic nematode species. However, it has never been determined whether the observed deficits were due (i) to the presence of null alleles, (ii) to a high level of consanguinity and/or (iii) to a Wahlund effect. The aim of the present work was, while taking into the possible confounding effect of null alleles, to disentangle consanguinity and Wahlund effect in natural populations of those three economically important cyst nematodes using microsatellite markers:Globodera pallida,G.tabacumandHeterodera schachtii, pests of potato, tobacco and sugar beet, respectively. The results show a consistent pattern of heterozygote deficiency in the three nematode species sampled at the spatial scale of the host plant. We demonstrate that the prevalence of null alleles is weak and that heterozygote deficits do not have a single origin. Our results suggested that it is restricted dispersal that leads to heterozygote deficits through both consanguinity and substructure, which effects can be linked to soil movement, cyst density, and the number of generations per year. We discuss potential implications for the durability of plant resistances that are used to protect crops against parasites in which mating between relatives occur. While consanguineous mating leads to homozygosity at all loci, including loci governing avirulence/virulence, which favours the expression of virulence when recessive, the Wahlund effect is expected to have no particular effect on the adaptation of nematodes to resistances.

AB - Deviations of genotypic frequencies from Hardy–Weinberg equilibrium (HWE) expectations could reveal important aspects of the biology of populations. Deviations from HWE due to heterozygote deficits have been recorded for three plant-parasitic nematode species. However, it has never been determined whether the observed deficits were due (i) to the presence of null alleles, (ii) to a high level of consanguinity and/or (iii) to a Wahlund effect. The aim of the present work was, while taking into the possible confounding effect of null alleles, to disentangle consanguinity and Wahlund effect in natural populations of those three economically important cyst nematodes using microsatellite markers:Globodera pallida,G.tabacumandHeterodera schachtii, pests of potato, tobacco and sugar beet, respectively. The results show a consistent pattern of heterozygote deficiency in the three nematode species sampled at the spatial scale of the host plant. We demonstrate that the prevalence of null alleles is weak and that heterozygote deficits do not have a single origin. Our results suggested that it is restricted dispersal that leads to heterozygote deficits through both consanguinity and substructure, which effects can be linked to soil movement, cyst density, and the number of generations per year. We discuss potential implications for the durability of plant resistances that are used to protect crops against parasites in which mating between relatives occur. While consanguineous mating leads to homozygosity at all loci, including loci governing avirulence/virulence, which favours the expression of virulence when recessive, the Wahlund effect is expected to have no particular effect on the adaptation of nematodes to resistances.

KW - consanguinity

KW - heterozygote deficit

KW - microsatellite

KW - nematode

KW - null allele

KW - Wahlund effect

U2 - 10.1111/mec.13142

DO - 10.1111/mec.13142

M3 - Article

VL - 24

SP - 1654

EP - 1677

JO - Molecular Ecology

JF - Molecular Ecology

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Montarry J, Pierre-Loup J, Gracianne C, Overall A, Bardou-Valette S, Olivier E et al. Heterozygote deficits in cyst plant-parasitic nematodes: possible causes and consequences. Molecular Ecology. 2015 Apr 3;24(8):1654-1677. https://doi.org/10.1111/mec.13142