Variation in resistance to multiple pathogen species: anther smuts of <i><scp>S</scp>ilene uniflora</i>

Chung, Erin; Petit, Elsa; Antonovics, Janis; Pedersen, Amy B.; Hood, Michael E.

doi:10.1002/ece3.346

Cited by 28 publications

(39 citation statements)

References 60 publications

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“…Plants can have highly specific defenses that could lead to apparent competition, effective against only one of two closely related pathogens (Chung et al 2012). Recent studies have demonstrated patterns of exclusion of new infections by existing viral infections, even when time of inoculation between the two variants was as short as 6 h (e.g., Julve et al 2013).…”

Section: Discussionmentioning

confidence: 99%

Interactions Within Susceptible Hosts Drive Establishment of Genetically Distinct Variants of an Insect-Borne Pathogen

et al. 2015

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Coinfections are common, leading to pathogen interactions during transmission and establishment in a host. However, few studies have tested the relative strengths of pathogen interactions in vectors and hosts that determine the outcome of infection. We tested interactions between two genetically distinct variants of the mealybug-transmitted Grapevine leafroll-associated virus 3. The transmission efficiency of each variant in single variant inoculations by two vector species was determined. The effects of vector species, a coinfected source, and simultaneous inoculation from multiple hosts to one host on variant establishment were examined. Within-vector interactions could have a role in transmission from hosts containing mixed infections, but not when vectors were moved from separate singly infected source plants to a single recipient plant. The invasive Planococcus ficus (Signoret) was a more efficient vector than Pseudococcus viburni (Signoret). Transmission efficiency of the two variants did not differ in single variant inoculations. Overall infections were the same whether from singly or coinfected source plants. In mixed inoculations, establishment of one variant was reduced. Mixed inoculations from two singly infected source plants resulted in fewer mixed infections than expected by chance. Therefore, the observed outcome was determined subsequent to host inoculation rather than in the vector. The outcome may be due to resource competition between pathogens. Alternatively apparent competition may be responsible; the pathogens' differential ability to overcome host defenses and colonize the host may determine the final outcome of new infections. Detailed knowledge of interactions between pathogens during transmission and establishment could improve understanding and management of disease spread.

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Section: Discussionmentioning

confidence: 99%

Interactions Within Susceptible Hosts Drive Establishment of Genetically Distinct Variants of an Insect-Borne Pathogen

et al. 2015

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“…A sampling site was defined as a location in which samples were collected a few metres apart. Sampling was performed by numerous investigators throughout Europe and was carried out as part of general disease surveys, other field trips, or as part of more formal investigations (Chung et al., ; Le Gac, Hood, Fournier et al., ; J. Abbate & J. Antonovics, unpublished studies). Within sampling sites, a single diseased flower was collected per individual plant, stored in silica gel, and DNA from the diploid teliospores was extracted for genetic analyses.…”

Section: Methodsmentioning

confidence: 99%

“…One explanation for coexistence of these three fungal species could be that they are allopatric, although they have been found to co‐occur in the same sites (Abbate & Antonovics, ; Chung, Petit, Antonovics, Pedersen, & Hood, ; Le Gac, Hood, Fournier et al., ); however, sampling has been limited thus far, and it remains possible that contact zones of allopatric distributions were sampled. An alternative hypothesis is that the species display differential specialization towards S. vulgaris versus S. uniflora .…”

Section: Introductionmentioning

confidence: 99%

“…An alternative hypothesis is that the species display differential specialization towards S. vulgaris versus S. uniflora . Previous studies further suggest that this hypothesis is unlikely, given that both host species have been found to be parasitized in nature by at least two of the Microbotryum species also parasitizing S. vulgaris : M. lagerheimii and M. silenes‐inflatae (Chung et al., ; Smith, Lutz, Ziegler, & Piątek, ).…”

Section: Introductionmentioning

confidence: 99%

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Co‐occurrence among three divergent plant‐castrating fungi in the same Silene host species

et al. 2018

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The competitive exclusion principle postulates that different species can only coexist in sympatry if they occupy distinct ecological niches. The goal of this study was to understand the geographical distribution of three species of Microbotryum anther-smut fungi that are distantly related but infect the same host plants, the sister species Silene vulgaris and S. uniflora, in Western Europe. We used microsatellite markers to investigate pathogen distribution in relation to host specialization and ecological factors. Microbotryum violaceo-irregulare was only found on S. vulgaris at high elevations in the Alps. Microbotryum lagerheimii could be subdivided into two genetically differentiated clusters, one on S. uniflora in the UK and the second on S. vulgaris in the Alps and Pyrenees. The most abundant pathogen species, M. silenes-inflatae, could be subdivided into four genetic clusters, co-occurring in the Alps, the UK and the Pyrenees, and was found on both S. vulgaris and S. uniflora. All three fungal species had high levels of homozygosity, in agreement with the selfing mating system generally observed in anther-smut fungi. The three pathogen species and genetic clusters had large range overlaps, but occurred at sites with different elevations, temperatures and precipitation levels. The three Microbotryum species thus do not appear to be maintained by host specialization or geographic allopatry, but instead may occupy different ecological niches in terms of environmental conditions.

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“…Intrahost competitive exclusion may also be important and is well documented among Microbotryum strains, including within‐ and among‐species interactions (Fortuna et al, ; Gold et al, ; Hood, ). Studies have indicated heritable variation in anther‐smut disease resistance (Alexander & Maltby, ; Cafuir, Antonovics, & Hood, ; Carlsson‐Granér & Pettersson, ; Chung, Petit, Antonovics, Pedersen, & Hood, ), but the mechanisms of resistance and whether it is inducible have not been determined.…”

Section: Discussionmentioning

confidence: 99%

Sympatry and interference of divergent Microbotryum pathogen species

Hood

Antonovics

Wolf

et al. 2019

Ecology and Evolution

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The impact of infectious diseases in natural ecosystems is strongly influenced by the degree of pathogen specialization and by the local assemblies of potential host species. This study investigated anther‐smut disease, caused by fungi in the genus Microbotryum , among natural populations of plants in the Caryophyllaceae. A broad geographic survey focused on sites of the disease on multiple host species in sympatry. Analysis of molecular identities for the pathogens revealed that sympatric disease was most often due to co‐occurrence of distinct, host‐specific anther‐smut fungi, rather than localized cross‐species disease transmission. Flowers from sympatric populations showed that the Microbotryum spores were frequently moved between host species. Experimental inoculations to simulate cross‐species exposure to the pathogens in these plant communities showed that the anther‐smut pathogen was less able to cause disease on its regular host when following exposure of the plants to incompatible pathogens from another host species. These results indicate that multi‐host/multi‐pathogen communities are common in this system and they involve a previously hidden mechanism of interference between Microbotryum fungi, which likely affects both pathogen and host distributions.

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Variation in resistance to multiple pathogen species: anther smuts of Silene uniflora

Cited by 28 publications

References 60 publications

Interactions Within Susceptible Hosts Drive Establishment of Genetically Distinct Variants of an Insect-Borne Pathogen

Interactions Within Susceptible Hosts Drive Establishment of Genetically Distinct Variants of an Insect-Borne Pathogen

Co‐occurrence among three divergent plant‐castrating fungi in the same Silene host species

Sympatry and interference of divergent Microbotryum pathogen species

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