Most cited article - PubMed ID 30420746
Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle
Mycena s.s. is a ubiquitous mushroom genus whose members degrade multiple dead plant substrates and opportunistically invade living plant roots. Having sequenced the nuclear genomes of 24 Mycena species, we find them to defy the expected patterns for fungi based on both their traditionally perceived saprotrophic ecology and substrate specializations. Mycena displayed massive genome expansions overall affecting all gene families, driven by novel gene family emergence, gene duplications, enlarged secretomes encoding polysaccharide degradation enzymes, transposable element (TE) proliferation, and horizontal gene transfers. Mainly due to TE proliferation, Arctic Mycena species display genomes of up to 502 Mbp (2-8× the temperate Mycena), the largest among mushroom-forming Agaricomycetes, indicating a possible evolutionary convergence to genomic expansions sometimes seen in Arctic plants. Overall, Mycena show highly unusual, varied mosaic-like genomic structures adaptable to multiple lifestyles, providing genomic illustration for the growing realization that fungal niche adaptations can be far more fluid than traditionally believed.
- Keywords
- Arctic biology, TE proliferation, biotrophy–saprotrophy evolution, carbon degradation, fungal genomics, fungal guild, genome size diversity, plant-fungus interactions, root-associations, saprotrophs,
- MeSH
- Agaricales * genetics MeSH
- Phylogeny MeSH
- Genome, Fungal * genetics MeSH
- Evolution, Molecular MeSH
- Gene Transfer, Horizontal MeSH
- Plants microbiology genetics MeSH
- DNA Transposable Elements genetics MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- DNA Transposable Elements MeSH
The white truffle (Tuber magnatum Picco.; WT) is the most expensive and arguably also the most delicious species within the genus Tuber. Due to its hidden belowground life cycle, complex host symbiosis, and yet unknown distribution, cultivation of the enigmatic species has only recently been achieved at some plantations in France. A sustainable production of WTs under future climate change, however, requires a better ecological understanding of the species' natural occurrence. Here, we combine information from truffle hunters with a literature review to assess the climatic, edaphic, geographic, and symbiotic characteristics of 231 reported WT sites in southeast Europe. Our meta-study shows that 75% of the WT sites are located outside the species' most famous harvest region, the Piedmont in northern Italy. Spanning a wide geographic range from ~ 37° N in Sicily to ~ 47° N in Hungary, and elevations between sea level in the north and 1000 m asl in the south, all WT sites are characterised by mean winter temperatures > 0.4 °C and summer precipitation totals of ~ 50 mm. Often formed during past flood or landslide events, current soil conditions of the WT sites exhibit pH levels between 6.4 and 8.7, high macroporosity, and a cation exchange capacity of ~ 17 meq/100 g. At least 26 potential host species from 12 genera were reported at the WT sites, with Populus alba and Quercus cerris accounting for 23.5% of all plant species. We expect our findings to contribute to a sustainable WT industry under changing environmental and economic conditions.
- Keywords
- Ectomycorrhiza, Environmental change, Fungi, Global warming, Non-woody forest products, Truffle cultivation,
- MeSH
- Ascomycota * MeSH
- Mycorrhizae * MeSH
- Soil MeSH
- Symbiosis MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Soil MeSH
Burgundy truffles are heterothallic ascomycetes that grow in symbiosis with trees. Despite their esteemed belowground fruitbodies, the species' complex lifecycle is still not fully understood. Here, we present the genetic patterns in three natural Burgundy truffle populations based on genotyped fruitbodies, ascospore extracts and ectomycorrhizal root tips using microsatellites and the mating-type locus. Distinct genetic structures with high relatedness in close vicinity were found for females (forming the fruitbodies) and males (fertilizing partner as inferred from ascospore extracts), with high genotypic diversity and annual turnover of males, suggesting that ephemeral male mating partners are germinating ascospores from decaying fruitbodies. The presence of hermaphrodites and the interannual persistence of a few males suggest that persistent mycelia may sporadically also act as males. Only female or hermaphroditic individuals were detected on root tips. At one site, fruitbodies grew in a fairy ring formed by a large female individual that showed an outward growth rate of 30 cm per year, with the mycelium decaying within the ring and being fertilized by over 50 male individuals. While fairy ring structures have never been shown for truffles, the genetics of Burgundy truffle populations support a similar reproductive biology as those of other highly prized truffles.
- MeSH
- Ascomycota * genetics MeSH
- Humans MeSH
- Mycorrhizae * genetics MeSH
- Life Cycle Stages MeSH
- Symbiosis MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Male MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition in terrestrial ecosystems. Mycorrhizal symbioses arose repeatedly across multiple lineages of Mucoromycotina, Ascomycota, and Basidiomycota. Considerable variation exists in the capacity of mycorrhizal fungi to acquire carbon from soil organic matter. Here, we present a combined analysis of 135 fungal genomes from 73 saprotrophic, endophytic and pathogenic species, and 62 mycorrhizal species, including 29 new mycorrhizal genomes. This study samples ecologically dominant fungal guilds for which there were previously no symbiotic genomes available, including ectomycorrhizal Russulales, Thelephorales and Cantharellales. Our analyses show that transitions from saprotrophy to symbiosis involve (1) widespread losses of degrading enzymes acting on lignin and cellulose, (2) co-option of genes present in saprotrophic ancestors to fulfill new symbiotic functions, (3) diversification of novel, lineage-specific symbiosis-induced genes, (4) proliferation of transposable elements and (5) divergent genetic innovations underlying the convergent origins of the ectomycorrhizal guild.
- MeSH
- Ecosystem MeSH
- Fungal Proteins genetics MeSH
- Phylogeny MeSH
- Plant Physiological Phenomena MeSH
- Genome, Fungal * MeSH
- Fungi classification genetics physiology MeSH
- Evolution, Molecular MeSH
- Mycorrhizae classification genetics physiology MeSH
- Plants microbiology MeSH
- Symbiosis * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Names of Substances
- Fungal Proteins MeSH