Haplotype-resolved genomes of Phlebopus portentosus reveal nuclear differentiation, TE-mediated variation, and saprotrophic potential

Summary

Scientists sequenced the complete genomes of two compatible strains of the king bolete mushroom (Phlebopus portentosus), an important edible and medicinal species. The study found that mobile DNA elements called transposons play a major role in creating genetic differences between the two fungal nuclei and in generating the diversity of compounds that give mushrooms their health benefits. The research shows this mushroom can both partner with trees and break down organic material on its own, making it uniquely adaptable.

Background

Phlebopus portentosus is the only Boletales species currently cultivated on an industrial scale and is widely consumed as an edible mushroom with significant nutritional and medicinal properties. Despite its economic importance, the trophic strategy and genomic adaptations of this species remain poorly understood. The debate continues regarding whether P. portentosus is ectomycorrhizal or saprotrophic, based on conflicting evidence from previous studies.

Objective

This study aims to generate high-quality, chromosome-level genome assemblies for two sexually compatible monokaryons of P. portentosus and conduct comparative genomic analysis to reveal nuclear differentiation, transposable element-mediated variation, and the species’ trophic strategy. The research seeks to elucidate the role of transposable elements in driving genome plasticity and metabolic diversity.

Results

The assemblies revealed genome sizes of 30.87 Mb (PP78) and 32.04 Mb (PP85), with 1.17 Mb difference primarily due to transposable element expansion in PP85. Comparative analysis identified 187 PP78-specific and 236 PP85-specific genes, with transposable elements driving structural variations and secondary metabolite gene cluster reorganization. The species displays genomic signatures of both ectomycorrhizal symbiosis and saprotrophic lifestyle.

Conclusion

This study demonstrates that transposable elements are major drivers of genome plasticity, nuclear divergence, and metabolic diversity in P. portentosus. The genomic evidence supports a facultative ectomycorrhizal lifestyle with expanded saprotrophic potential. The high-quality reference genomes provide valuable resources for further cultivation optimization and metabolic engineering of this economically important species.
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