Demographic and genetic impacts of powdery mildew in a young oak (Quercus robur L.) cohort

Abstract Key message By monitoring a field experiment over nine years, we investigated the impacts of the two main pathogen species Erysiphe quercicola S. Takam. and U. Braun and Erysiphe alphitoides (Griffon and Maubl.) U. Braun and S. Takam causing powdery mildew on a young cohort of pedunculate o...

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Main Authors: Benoit Barrès, Cyril Dutech, Gilles Saint-Jean, Catherine Bodénès, Christian Burban, Virgil Fiévet, Camille Lepoittevin, Pauline Garnier-Géré, Marie-Laure Desprez-Loustau
Format: Article
Language:English
Published: BMC 2024-10-01
Series:Annals of Forest Science
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Online Access:https://doi.org/10.1186/s13595-024-01259-2
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author Benoit Barrès
Cyril Dutech
Gilles Saint-Jean
Catherine Bodénès
Christian Burban
Virgil Fiévet
Camille Lepoittevin
Pauline Garnier-Géré
Marie-Laure Desprez-Loustau
author_facet Benoit Barrès
Cyril Dutech
Gilles Saint-Jean
Catherine Bodénès
Christian Burban
Virgil Fiévet
Camille Lepoittevin
Pauline Garnier-Géré
Marie-Laure Desprez-Loustau
author_sort Benoit Barrès
collection DOAJ
description Abstract Key message By monitoring a field experiment over nine years, we investigated the impacts of the two main pathogen species Erysiphe quercicola S. Takam. and U. Braun and Erysiphe alphitoides (Griffon and Maubl.) U. Braun and S. Takam causing powdery mildew on a young cohort of pedunculate oak (Quercus robur L.), both from a demographic and genetic point of view using SNP markers. We show that survival rate is affected by mean disease severity. But while the growth-related tolerance to infection of the oak individual seems to be more determinant than resistance against infection, no equalizing effect of the disease could be detected. Context Studies on the effects of pathogens on the survival and population dynamics of forest trees are scarce. Yet a better understanding of these interactions could prove strategic in the challenging context of climate change. Aims Our general objective was to characterize the demographic and genetic impact of the two main pathogen species Erysiphe quercicola S. Takam. and U. Braun and Erysiphe alphitoides (Griffon and Maubl.) U. Braun and S. Takam causing powdery mildew in the early stages of a Quercus robur L. population. Methods An ad hoc field design with two disease exposures, natural and protected, was surveyed over nine years. This enabled a detailed phenotypic monitoring of 1733 emerging individuals from 15 progenies, and the genotyping of 68% of them. Results The pathogen induced high levels of seedling mortality several years after sowing, associated with reduced growth and capacity to overwinter. Fast-growing families showed the highest survival rate under both natural and protected disease exposure. Contrary to a possible trade-off hypothesis between growth and defense, family height potential was not negatively related to disease resistance across the studied oak mother trees. While supporting a deleterious effect of very low individual heterozygosity on the probability of survival, average genomic diversity was not significantly affected by mortality associated with powdery mildew. Our study also points to a few candidate genes for several fitness-related traits. Conclusion Overall, our results suggest that in oak natural populations, infection levels (related to resistance sensu stricto) may be less determinant than growth-related tolerance to infection for the fate of seedlings. However, an equalizing effect of powdery mildew on relative oak genotype performances cannot be excluded at later stages.
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spelling doaj-art-e165c8efae4d4d9daa7a16affd50edb52025-08-20T02:17:52ZengBMCAnnals of Forest Science1297-966X2024-10-0181113310.1186/s13595-024-01259-2Demographic and genetic impacts of powdery mildew in a young oak (Quercus robur L.) cohortBenoit Barrès0Cyril Dutech1Gilles Saint-Jean2Catherine Bodénès3Christian Burban4Virgil Fiévet5Camille Lepoittevin6Pauline Garnier-Géré7Marie-Laure Desprez-Loustau8INRAE, Univ. Bordeaux, BIOGECOINRAE, Univ. Bordeaux, BIOGECOINRAE, Univ. Bordeaux, BIOGECOINRAE, Univ. Bordeaux, BIOGECOINRAE, Univ. Bordeaux, BIOGECOINRAE, Univ. Bordeaux, BIOGECOINRAE, Univ. Bordeaux, BIOGECOINRAE, Univ. Bordeaux, BIOGECOINRAE, Univ. Bordeaux, BIOGECOAbstract Key message By monitoring a field experiment over nine years, we investigated the impacts of the two main pathogen species Erysiphe quercicola S. Takam. and U. Braun and Erysiphe alphitoides (Griffon and Maubl.) U. Braun and S. Takam causing powdery mildew on a young cohort of pedunculate oak (Quercus robur L.), both from a demographic and genetic point of view using SNP markers. We show that survival rate is affected by mean disease severity. But while the growth-related tolerance to infection of the oak individual seems to be more determinant than resistance against infection, no equalizing effect of the disease could be detected. Context Studies on the effects of pathogens on the survival and population dynamics of forest trees are scarce. Yet a better understanding of these interactions could prove strategic in the challenging context of climate change. Aims Our general objective was to characterize the demographic and genetic impact of the two main pathogen species Erysiphe quercicola S. Takam. and U. Braun and Erysiphe alphitoides (Griffon and Maubl.) U. Braun and S. Takam causing powdery mildew in the early stages of a Quercus robur L. population. Methods An ad hoc field design with two disease exposures, natural and protected, was surveyed over nine years. This enabled a detailed phenotypic monitoring of 1733 emerging individuals from 15 progenies, and the genotyping of 68% of them. Results The pathogen induced high levels of seedling mortality several years after sowing, associated with reduced growth and capacity to overwinter. Fast-growing families showed the highest survival rate under both natural and protected disease exposure. Contrary to a possible trade-off hypothesis between growth and defense, family height potential was not negatively related to disease resistance across the studied oak mother trees. While supporting a deleterious effect of very low individual heterozygosity on the probability of survival, average genomic diversity was not significantly affected by mortality associated with powdery mildew. Our study also points to a few candidate genes for several fitness-related traits. Conclusion Overall, our results suggest that in oak natural populations, infection levels (related to resistance sensu stricto) may be less determinant than growth-related tolerance to infection for the fate of seedlings. However, an equalizing effect of powdery mildew on relative oak genotype performances cannot be excluded at later stages.https://doi.org/10.1186/s13595-024-01259-2Pedunculate oakOak regenerationDisease-diversity relationshipTrade-off
spellingShingle Benoit Barrès
Cyril Dutech
Gilles Saint-Jean
Catherine Bodénès
Christian Burban
Virgil Fiévet
Camille Lepoittevin
Pauline Garnier-Géré
Marie-Laure Desprez-Loustau
Demographic and genetic impacts of powdery mildew in a young oak (Quercus robur L.) cohort
Annals of Forest Science
Pedunculate oak
Oak regeneration
Disease-diversity relationship
Trade-off
title Demographic and genetic impacts of powdery mildew in a young oak (Quercus robur L.) cohort
title_full Demographic and genetic impacts of powdery mildew in a young oak (Quercus robur L.) cohort
title_fullStr Demographic and genetic impacts of powdery mildew in a young oak (Quercus robur L.) cohort
title_full_unstemmed Demographic and genetic impacts of powdery mildew in a young oak (Quercus robur L.) cohort
title_short Demographic and genetic impacts of powdery mildew in a young oak (Quercus robur L.) cohort
title_sort demographic and genetic impacts of powdery mildew in a young oak quercus robur l cohort
topic Pedunculate oak
Oak regeneration
Disease-diversity relationship
Trade-off
url https://doi.org/10.1186/s13595-024-01259-2
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