Multiple infections, relatedness and virulence in the anther‐smut fungus castrating Saponaria plants

Multiple infections (co‐occurrence of multiple pathogen genotypes within an individual host) can have important impacts on diseases. Relatedness among pathogens can affect the likelihood of multiple infections and their consequences through kin selection. Previous studies on the castrating anther‐sm...

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Published inMolecular ecology Vol. 27; no. 23; pp. 4947 - 4959
Main Authors Fortuna, Taiadjana M., Namias, Alice, Snirc, Alodie, Branca, Antoine, Hood, Michael E., Raquin, Christian, Shykoff, Jacqui A., Giraud, Tatiana
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.12.2018
Wiley
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Abstract Multiple infections (co‐occurrence of multiple pathogen genotypes within an individual host) can have important impacts on diseases. Relatedness among pathogens can affect the likelihood of multiple infections and their consequences through kin selection. Previous studies on the castrating anther‐smut fungus Microbotryum lychnidis‐dioicae have shown that multiple infections occur in its host plant Silene latifolia. Relatedness was high among fungal genotypes within plants, which could result from competitive exclusion between unrelated fungal genotypes, from population structure or from interactions between plant and fungal genotypes for infection ability. Here, we aimed at disentangling these hypotheses using M. saponariae and its host Saponaria officinalis, both experimentally tractable for these questions. By analysing populations using microsatellite markers, we also found frequent occurrence of multiple infections and high relatedness among strains within host plants. Infections resulting from experimental inoculations in the greenhouse also revealed high relatedness among strains co‐infecting host plants, even in clonally replicated plant genotypes, indicating that high relatedness within plants did not result merely from plant x fungus interactions or population structure. Furthermore, hyphal growth in vitro was affected by the presence of a competitor growing nearby and by its genetic similarity, although this latter effect was strain‐dependent. Altogether, our results support the hypothesis that relatedness‐dependent competitive exclusion occurs in Microbotryum fungi within plants. These microorganisms can thus respond to competitors and to their level of relatedness.
AbstractList Abstract Multiple infections (co‐occurrence of multiple pathogen genotypes within an individual host) can have important impacts on diseases. Relatedness among pathogens can affect the likelihood of multiple infections and their consequences through kin selection. Previous studies on the castrating anther‐smut fungus Microbotryum lychnidis‐dioicae have shown that multiple infections occur in its host plant Silene latifolia . Relatedness was high among fungal genotypes within plants, which could result from competitive exclusion between unrelated fungal genotypes, from population structure or from interactions between plant and fungal genotypes for infection ability. Here, we aimed at disentangling these hypotheses using M. saponariae and its host Saponaria officinalis , both experimentally tractable for these questions. By analysing populations using microsatellite markers, we also found frequent occurrence of multiple infections and high relatedness among strains within host plants. Infections resulting from experimental inoculations in the greenhouse also revealed high relatedness among strains co‐infecting host plants, even in clonally replicated plant genotypes, indicating that high relatedness within plants did not result merely from plant x fungus interactions or population structure. Furthermore, hyphal growth in vitro was affected by the presence of a competitor growing nearby and by its genetic similarity, although this latter effect was strain‐dependent. Altogether, our results support the hypothesis that relatedness‐dependent competitive exclusion occurs in Microbotryum fungi within plants. These microorganisms can thus respond to competitors and to their level of relatedness.
Multiple infections (co‐occurrence of multiple pathogen genotypes within an individual host) can have important impacts on diseases. Relatedness among pathogens can affect the likelihood of multiple infections and their consequences through kin selection. Previous studies on the castrating anther‐smut fungus Microbotryum lychnidis‐dioicae have shown that multiple infections occur in its host plant Silene latifolia. Relatedness was high among fungal genotypes within plants, which could result from competitive exclusion between unrelated fungal genotypes, from population structure or from interactions between plant and fungal genotypes for infection ability. Here, we aimed at disentangling these hypotheses using M. saponariae and its host Saponaria officinalis, both experimentally tractable for these questions. By analysing populations using microsatellite markers, we also found frequent occurrence of multiple infections and high relatedness among strains within host plants. Infections resulting from experimental inoculations in the greenhouse also revealed high relatedness among strains co‐infecting host plants, even in clonally replicated plant genotypes, indicating that high relatedness within plants did not result merely from plant x fungus interactions or population structure. Furthermore, hyphal growth in vitro was affected by the presence of a competitor growing nearby and by its genetic similarity, although this latter effect was strain‐dependent. Altogether, our results support the hypothesis that relatedness‐dependent competitive exclusion occurs in Microbotryum fungi within plants. These microorganisms can thus respond to competitors and to their level of relatedness.
Multiple infections (co-occurrence of multiple pathogen genotypes within an individual host) can have important impacts on diseases. Relatedness among pathogens can affect the likelihood of multiple infections and their consequences through kin selection. Previous studies on the castrating anther-smut fungus Microbotryum lych-nidis-dioicae have shown that multiple infections occur in its host plant Silene latifolia. Relatedness was high among fungal genotypes within plants, which could result from competitive exclusion between unrelated fungal genotypes, from population structure or from interactions between plant and fungal genotypes for infection ability. Here, we aimed at disentangling these hypotheses using M. saponariae and its host Saponaria officinalis, both experimentally tractable for these questions. By analysing populations using microsatellite markers, we also found frequent occurrence of multiple infections and high relatedness among strains within host plants. Infections resulting from experimental inoculations in the greenhouse also revealed high relatedness among strains co-infecting host plants, even in clonally replicated plant genotypes, indicating that high relatedness within plants did not result merely from plant x fungus interactions or population structure. Furthermore, hyphal growth in vitro was affected by the presence of a competitor growing nearby and by its genetic similarity, although this latter effect was strain-dependent. Altogether, our results support the hypothesis that relatedness-dependent competitive exclusion occurs in Microbotryum fungi within plants. These micro organisms can thus respond to competitors and to their level of relatedness. K E Y W O R D S hyphae, virulence, kin selection, sterilizing pathogen, vegetative incompatibility
Multiple infections (co‐occurrence of multiple pathogen genotypes within an individual host) can have important impacts on diseases. Relatedness among pathogens can affect the likelihood of multiple infections and their consequences through kin selection. Previous studies on the castrating anther‐smut fungus Microbotryum lychnidis‐dioicae have shown that multiple infections occur in its host plant Silene latifolia. Relatedness was high among fungal genotypes within plants, which could result from competitive exclusion between unrelated fungal genotypes, from population structure or from interactions between plant and fungal genotypes for infection ability. Here, we aimed at disentangling these hypotheses using M. saponariae and its host Saponaria officinalis, both experimentally tractable for these questions. By analysing populations using microsatellite markers, we also found frequent occurrence of multiple infections and high relatedness among strains within host plants. Infections resulting from experimental inoculations in the greenhouse also revealed high relatedness among strains co‐infecting host plants, even in clonally replicated plant genotypes, indicating that high relatedness within plants did not result merely from plant x fungus interactions or population structure. Furthermore, hyphal growth in vitro was affected by the presence of a competitor growing nearby and by its genetic similarity, although this latter effect was strain‐dependent. Altogether, our results support the hypothesis that relatedness‐dependent competitive exclusion occurs in Microbotryum fungi within plants. These microorganisms can thus respond to competitors and to their level of relatedness.
Author Giraud, Tatiana
Branca, Antoine
Shykoff, Jacqui A.
Snirc, Alodie
Raquin, Christian
Fortuna, Taiadjana M.
Namias, Alice
Hood, Michael E.
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Issue 23
Keywords hyphae
vegetative incompatibility
sterilizing pathogen
virulence
kin selection
Language English
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Snippet Multiple infections (co‐occurrence of multiple pathogen genotypes within an individual host) can have important impacts on diseases. Relatedness among...
Multiple infections (co-occurrence of multiple pathogen genotypes within an individual host) can have important impacts on diseases. Relatedness among...
Abstract Multiple infections (co‐occurrence of multiple pathogen genotypes within an individual host) can have important impacts on diseases. Relatedness among...
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StartPage 4947
SubjectTerms Biodiversity
Competition
Fungi
Genetic markers
Genotypes
Host plants
hyphae
Infections
Kin selection
Life Sciences
Microbotryum
Microorganisms
Microsatellites
Pathogens
Population structure
Populations and Evolution
Smut
sterilizing pathogen
Strains (organisms)
vegetative incompatibility
Virulence
Title Multiple infections, relatedness and virulence in the anther‐smut fungus castrating Saponaria plants
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fmec.14911
https://www.ncbi.nlm.nih.gov/pubmed/30372557
https://www.proquest.com/docview/2158010993
https://search.proquest.com/docview/2127198345
https://hal.science/hal-01921820
Volume 27
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