Diploid-dominant life cycles characterize the early evolution of Fungi | Proceedings of the National Academy of Sciences

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• major evolutionary trends in the non-Dikarya fungi by phylogenomic analysis of 69 newly generated draft genome sequences of the zoosporic (flagellated) lineages of true fungi

• The resulting k-mer and allele frequency (AF) histograms (SI Appendix, Fig. S8) were systematically binned by ploidy based on their similarity to canonical examples of k-mer (Fig. 3A) and AF (Fig. 3B) histograms, in addition to measured density of heterozygous positions (i.e., single-nucleotide polymorphisms [SNPs]) postfiltering.

• It has been assumed that fungi are characterized by a haploid-dominant life cycle with a general absence of mitosis in the diploid stage (haplontic life cycles)

• We show, using the estimated heterozygosity of these genomes, that many fungal lineages have diploid-dominant life cycles (diplontic). This finding forces us to rethink the early evolution of the fungal cell.

• Most of the described species in kingdom Fungi are contained in two phyla, the Ascomycota and the Basidiomycota (subkingdom Dikarya)

• but the phylogeny and genetic characteristics of most of these lineages are poorly understood due to limited genome sampling.

• heterozygosity based on genome sequence data indicate that the zoosporic lineages plus the Zoopagomycota are frequently characterized by diploid-dominant life cycles

• apped additional traits, such as ancestral cell-cycle regulators, cell-membrane– and cell-wall–associated genes, and the use of the amino acid selenocysteine on the phylogeny and found that these ancestral traits that are shared with Metazoa have been subject to extensive parallel loss across zoosporic lineages.

• Fungi and Metazoa evolved from a common protist-like ancestor, yet the two kingdoms have diverged in ways that make their kinship as Opisthokonts barely recognizable.

• The two kingdoms are also considered intrinsically different in life cycles, because fungi are characterized as being haplontic (haploid-dominant life cycle) while animals are diplontic (diploid-dominant)

• m Dikarya, with the majority of fungal species diversity, comprises lineages that spend some or most of their life cycles in a dikaryotic phase wherein two haploid nuclei undergo conjugate division, a cell type genetically analogous to a diploid (3)

• arly-diverging fungal lineages (EDF),

• EDF have retained ancestral traits also retained in Metazoa, such as flagellation, actin structures used for crawling, presence of cholesterol in cell membranes, vitamin dependencies, and cell-cycle genes (4–8).

• lthough fungi are often considered to have haploid-dominant life cycles, there are many variations observed

• Overall, although we appreciate that fungal life cycles have great potential to vary, we have a poor understanding of life cycles of the EDF which represent the majority of the phylogenetic diversity of Fungi.

• EDF to comprise 11 phyla, including 8 zoosporic phyla that reproduce with swimming spores and form a contentious paraphyletic grade along the backbone of the fungal tree

• Mating and sexuality are poorly described in zoosporic fungi beyond the well-characterized water mold model Allomyces

• life cycles of Chytridiomycota are characterized as being haplontic with zygotic meiosis (27–29), but the majority of assumptions of meiotic stages are unconfirmed by cytology

• Our genome analyses provide a strongly supported phylogeny for understanding taxonomy and the evolution of ploidy and other traits which had previously been held to be distinctive between Fungi and Metazoa.

• hese data bolster the growing picture that many traits including motility, feeding modes, and life cycles changed gradually during the early diversification of fungi.