Host phenology and geography as drivers of differentiation in generalist fungal mycoparasites

Article

Pintye, Alexandra, Ropars, Jeanne, Harvey, Nick, Shin, Hyeon Dong, Leyronas, Christel, Nicot, Philippe C., Giraud, Tatiana and Kiss, Levente. 2015. "Host phenology and geography as drivers of differentiation in generalist fungal mycoparasites." PLoS One. 10 (3). https://doi.org/10.1371/journal.pone.0120703
Article Title

Host phenology and geography as drivers of differentiation in generalist fungal mycoparasites

ERA Journal ID39745
Article CategoryArticle
AuthorsPintye, Alexandra (Author), Ropars, Jeanne (Author), Harvey, Nick (Author), Shin, Hyeon Dong (Author), Leyronas, Christel (Author), Nicot, Philippe C. (Author), Giraud, Tatiana (Author) and Kiss, Levente (Author)
Journal TitlePLoS One
Journal Citation10 (3)
Number of Pages15
Year2015
PublisherPublic Library of Science (PLoS)
Place of PublicationUnited States
ISSN1932-6203
Digital Object Identifier (DOI)https://doi.org/10.1371/journal.pone.0120703
Abstract

The question as to why parasites remain generalist or become specialist is a key unresolved question in evolutionary biology. Ampelomyces spp., intracellular mycoparasites of powdery mildew fungi, which are themselves plant pathogens, are a useful model for studies of this issue. Ampelomyces is used for the biological control of mildew. Differences in mycohost phenology promote temporal isolation between sympatric Ampelomyces mycoparasites. Apple powdery mildew (APM) causes spring epidemics, whereas other powdery mildew species on plants other than apple cause epidemics later in the season. This has resulted in genetic differentiation between APM and non-APM strains. It is unclear whether there is genetic differentiation between non-APM Ampelomyces lineages due to their specialization on different mycohosts.We used microsatellites to address this question and found no significant differentiation between non-APM Ampelomyces strains from different mycohosts or host plants, but strong differentiation between APM and non-APM strains. A geographical structure was revealed in both groups, with differences between European countries, demonstrating restricted dispersal at the continent scale and a high resolution for our markers. We found footprints of recombination in both groups, possibly more frequent in the APM cluster. Overall, Ampelomyces thus appears to be one of the rare genuine generalist pathogenic fungi able to parasitize multiple hosts in natural populations. It is therefore an excellent model for studying the evolution of pathogens towards a generalist rather than host-specific strategy, particularly in light of the tritrophic interaction between Ampelomyces mycoparasites, their powdery mildew fungal hosts and the mildew host plants.

KeywordsAscomycota; fungal DNA; genetic variation; linkaged disequilibrium; microsatellite repeats; phylogeny; plant diseases; plants; microbiology: bacteriology, mycology, parasitology and virology; Ampelomyces spp.; apple powdery mildew
ANZSRC Field of Research 2020310805. Plant pathology
310705. Mycology
Public Notes

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Byline AffiliationsHungarian Academy of Sciences, Hungary
French National Centre for Scientific Research, France
Genetic Marker Services, United Kingdom
Korea University
National Research Institute for Agriculture, Food and Environment (INRAE), France
Institution of OriginUniversity of Southern Queensland
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Peach rusty spot is caused by the apple powdery mildew fungus, Podosphaera leucotricha
Jankovics, Tünde, Dolovac, Nenad, Bulajic, Aleksandra, Krstic, Branka, Pascal, Thierry, Bardin, Marc, Nicot, Philippe C. and Kiss, Levente. 2011. "Peach rusty spot is caused by the apple powdery mildew fungus, Podosphaera leucotricha." Plant Disease: an international journal of applied plant pathology. 95 (6), pp. 719-724. https://doi.org/10.1094/PDIS-10-10-0711
Limits of nuclear ribosomal DNA internal transcribed spacer (ITS) sequences as species barcodes for Fungi
Kiss, Levente. 2012. "Limits of nuclear ribosomal DNA internal transcribed spacer (ITS) sequences as species barcodes for Fungi." University of Adelaide. 109 (27), p. 1811. https://doi.org/10.1073/pnas.1207143109
Does the parasite follow its host? Occurrence of morphologically barely distinguishable powdery mildew anamorphs on Oenothera spp. in different parts of the world
Bereczky, Zsolt, Pintye, Alexandra, Csontos, Peter, Braun, Uwe and Kiss, Levente. 2015. "Does the parasite follow its host? Occurrence of morphologically barely distinguishable powdery mildew anamorphs on Oenothera spp. in different parts of the world." Mycoscience. 56 (3), pp. 267-272. https://doi.org/10.1016/j.myc.2014.08.001
First detection of tomato powdery mildew caused by Oidium neolycopersici in South Africa
Lebeda, A., Mieslerova, B., Jankovics, T., Kiss, L. and van der Linde, E. J.. 2015. "First detection of tomato powdery mildew caused by Oidium neolycopersici in South Africa." South African Journal of Botany. 99, pp. 153-157. https://doi.org/10.1016/j.sajb.2015.03.196
The evolution of species concepts and species recognition criteria in plant pathogenic fungi
Cai, Lei, Giraud, Tatiana, Zhang, Ning, Cai, Guohong, Begerow, Dominik and Shivas, Roger G.. 2011. "The evolution of species concepts and species recognition criteria in plant pathogenic fungi." Fungal Diversity. 50 (1), pp. 121-133. https://doi.org/10.1007/s13225-011-0127-8
Towards a universal barcode of oomycetes - a comparison of the cox1 and cox2 loci
Choi, Young Joon, Kruse, Julia, Nam, Bora, Nigrelli, Lisa, Telle, Sabine, Thines, Marco, Ploch, Sebastian, Beakes, Gordon, Glockling, Sally, Shin, Hyeon Dong, Shivas, Roger G. and Voglmayr, Hermann. 2015. "Towards a universal barcode of oomycetes - a comparison of the cox1 and cox2 loci." Molecular Ecology Resources. 15 (6), pp. 1275-1288. https://doi.org/10.1111/1755-0998.12398
Refining a method for ascospore viability testing in overwintering chasmothecia of Erysiphe necator
Vagi, Pal, Caffi, Tito, Vaczy, Kalman Zoltan, Nemeth, Mark Z. and Kiss, Levente. 2016. "Refining a method for ascospore viability testing in overwintering chasmothecia of Erysiphe necator." European Journal of Plant Pathology. 144 (4), pp. 799-802. https://doi.org/10.1007/s10658-015-0797-2
Sporulation rate in culture and mycoparasitic activity, but not mycohost specificity, are the key factors for selecting Ampelomyces strains for biocontrol of grapevine powdery mildew (Erysiphe necator)
Legler, Sara Elisabetta, Pintye, Alexandra, Caffi, Tito, Gulyas, Szilvia, Bohar, Gyula, Rossi, Vittorio and Kiss, Levente. 2016. "Sporulation rate in culture and mycoparasitic activity, but not mycohost specificity, are the key factors for selecting Ampelomyces strains for biocontrol of grapevine powdery mildew (Erysiphe necator)." European Journal of Plant Pathology. 144 (4), pp. 723-736. https://doi.org/10.1007/s10658-015-0834-1
Molecular identification and pathogenicity assessment of a rust fungus infecting common ragweed (Ambrosia artemisiifolia) in its native North American range
Kassai-Jager, Edit, Seier, Marion K., Evans, Harry C. and Kiss, Levente. 2016. "Molecular identification and pathogenicity assessment of a rust fungus infecting common ragweed (Ambrosia artemisiifolia) in its native North American range." European Journal of Plant Pathology. 145 (1), pp. 81-87. https://doi.org/10.1007/s10658-015-0815-4