Comparative genomics reveals the origin of fungal hyphae and multicellularity

Enikő Kiss, Botond Hegedüs, Máté Virágh, Torda Varga, Zsolt Merényi, Tamás Kószó, Balázs Bálint, Arun N. Prasanna, Krisztina Krizsán, Sándor Kocsubé, Meritxell Riquelme, Norio Takeshita and László G. Nagy ()
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Enikő Kiss: Institute of Biochemistry
Botond Hegedüs: Institute of Biochemistry
Máté Virágh: Institute of Biochemistry
Torda Varga: Institute of Biochemistry
Zsolt Merényi: Institute of Biochemistry
Tamás Kószó: Institute of Biochemistry
Balázs Bálint: Institute of Biochemistry
Arun N. Prasanna: Institute of Biochemistry
Krisztina Krizsán: Institute of Biochemistry
Sándor Kocsubé: University of Szeged, Faculty of Science and Informatics
Meritxell Riquelme: Centro de Investigación Científica y de Educación Superior de Ensenada
Norio Takeshita: University of Tsukuba
László G. Nagy: Institute of Biochemistry

Nature Communications, 2019, vol. 10, issue 1, 1-13

Abstract: Abstract Hyphae represent a hallmark structure of multicellular fungi. The evolutionary origins of hyphae and of the underlying genes are, however, hardly known. By systematically analyzing 72 complete genomes, we here show that hyphae evolved early in fungal evolution probably via diverse genetic changes, including co-option and exaptation of ancient eukaryotic (e.g. phagocytosis-related) genes, the origin of new gene families, gene duplications and alterations of gene structure, among others. Contrary to most multicellular lineages, the origin of filamentous fungi did not correlate with expansions of kinases, receptors or adhesive proteins. Co-option was probably the dominant mechanism for recruiting genes for hypha morphogenesis, while gene duplication was apparently less prevalent, except in transcriptional regulators and cell wall - related genes. We identified 414 novel gene families that show correlated evolution with hyphae and that may have contributed to its evolution. Our results suggest that hyphae represent a unique multicellular organization that evolved by limited fungal-specific innovations and gene duplication but pervasive co-option and modification of ancient eukaryotic functions.

Date: 2019
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DOI: 10.1038/s41467-019-12085-w

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