Periodic Reporting for period 4 - Multicellularity (The genetic basis of the convergent evolution of fungal multicellularity)
Reporting period: 2022-07-01 to 2023-06-30
We examine one of the big questions in biology, the genetic bases of major evolutionary transitions. One such transition is the evolution of multicellularity, which enabled the emergence of complex organisms from unicellular ones, including animals, plants as well as fungi. In fungi, multicellular growth is an economically important trait for two reasons. First, hyphal growth is a main pathogenicity factor of plant and animal pathogens, so understanding the evolutionary origins and genetic bases of hyphal growth will have potential implications in the fight against fungal infections. Second, complex multicellular fruiting bodies of fungi, known as mushrooms, represent an important and sustainable food source, which offers potential practical applications of the results generated during this project. Complex multicellularity of fruiting bodies is similar to the complexity level animals have reached also, and it follows that understanding the governing principles of fruiting body evolution may have implications for understanding other complex organisms also. The overall aims of the project are understanding the evolutionary / genetic origins of fungal multicellularity and placing fungi on the map of major evolutionary transitions. We focus on both hyphal growth and fruiting body development and identify key genetic changes by comparative genomic approaches, that allow us to look into the past and reconstruct the sequence of genetic events that accompanied the transition from unicellular to multicellular, as well as gene expression profiling (transcriptomic methods), which allow real-time readouts of gene expression (activity) changes during the formation of fruiting bodies.
We have reconstructed the evolution of fungal multicellularity and inferred gene families that underpin the emergence of multicellular fungi using whole genome datasets for 72 and 202 species. In the other pillar of the project, we obtained RNA-Seq data for multiple complex multicellular species (similar data for further species are now being generated). During the second half of the project, we comprehensively analyzed gene families associated with the evolution of multicellularity (Kiss et al 2019 Nature Comms, Merenyi et al 2023 Nature Ecol. Evol.) and extensively compared fungal multicellularity to that of animals and plants (Nagy et al 2020 Fungal Biology Reviews). We concluded that fungi followed a unique route to multicellular life, which differs from those of animals and plants. As a result, our work contributed to the rethinking of the general principles of the emergence of multicellular organisms during evolution. In the second pillar of the project, we identified shared, evolutionarily conserved genetic elements behind complex multicellularity. Our main approach here was comparative transcriptomics, which allowed us to define a core set of development-associated gene families in mushroom-forming fungi. This was published as a comprehensive monograph in 2023 (Studies in Mycology). Overall, the project achieves the goals set out in the Annex and contributed considerably to uncovering the molecular details of the multicellular life of fungi.
We have made progress in uncovering the genetic bases of fungal multicellularity. Multicellular growth in fungi has immense implications in pathogenic behaviour. Because of this, beyond the direct implications of our work in understanding major evolutionary transitions, the advances made during the project might have implications in understanding pathogenicity of fungi and eventually lead to better strategies for fighting fungal infections.