How the truffle got its mate: insights from genetic structure in spontaneous and planted Mediterranean populations of Tuber melanosporum

The life cycles and dispersal of edible fungi are still poorly known, thus limiting our understanding of their evolution and domestication. The prized Tuber melanosporum produces fruitbodies (fleshy organs where meiospores mature) gathered in natural, spontaneously inoculated forests or harvested in...

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Bibliographic Details
Published in:Molecular ecology 2016-11, Vol.25 (22), p.5611-5627
Main Authors: Taschen, E., Rousset, F., Sauve, M., Benoit, L., Dubois, M.-P., Richard, F., Selosse, M.-A.
Format: Article
Language:English
Subjects:
Ascomycota - genetics
Biodiversity and Ecology
dispersal
domestication
ectomycorrhizae
Environmental Sciences
Forests
France
Fungi
Genetic diversity
Genetic Variation
Genetics, Population
hermaphroditism
hypogeous fungi
inbreeding
Microsatellite Repeats
Mycorrhizae
Plant ecology
Population genetics
Soil Microbiology
Tuber
Tuber melanosporum
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Summary:The life cycles and dispersal of edible fungi are still poorly known, thus limiting our understanding of their evolution and domestication. The prized Tuber melanosporum produces fruitbodies (fleshy organs where meiospores mature) gathered in natural, spontaneously inoculated forests or harvested in plantations of nursery‐inoculated trees. Yet, how fruitbodies are formed remains unclear, thus limiting yields, and how current domestication attempts affect population genetic structure is overlooked. Fruitbodies result from mating between two haploid individuals: the maternal parent forms the flesh and the meiospores, while the paternal parent only contributes to the meiospores. We analyzed the genetic diversity of T. melanosporum comparatively in spontaneous forests vs. plantations, using SSR polymorphism of 950 samples from South‐East France. All populations displayed strong genetic isolation by distance at the metric scale, possibly due to animal dispersal, meiospore persistence in soil, and/or exclusion of unrelated individuals by vegetative incompatibility. High inbreeding was consistently found, suggesting that parents often develop from meiospores produced by the same fruitbody. Unlike maternal genotypes, paternal mycelia contributed to few fruitbodies each, did not persist over years, and were undetectable on tree mycorrhizae. Thus, we postulate that germlings from the soil spore bank act as paternal partners. Paternal genetic diversity and outbreeding were higher in plantations than in spontaneous truffle‐grounds, perhaps because truffle growers disperse fruitbodies to maintain inoculation in plantations. However, planted and spontaneous populations were not genetically isolated, so that T. melanosporum illustrates an early step of domestication where genetic structure remains little affected.
ISSN:0962-1083
1365-294X
DOI:10.1111/mec.13864