期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：36
DOI：10.1073/pnas.2116841119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
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). However, this characterization is based largely on information for Dikarya, a group of fungi that contains mushrooms, lichens, molds, yeasts, and most described fungi. We now appreciate that most early-diverging lineages of fungi are not Dikarya and share traits with protists, such as flagellated life stages. Here, we generated an improved phylogeny of the fungi by generating genome sequences of 69 zoosporic fungi. 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). As a result, our understanding of the biology of the kingdom is heavily influenced by traits observed in Dikarya, such as aerial spore dispersal and life cycles dominated by mitosis of haploid nuclei. We now appreciate that Fungi comprises numerous phylum-level lineages in addition to those of Dikarya, but the phylogeny and genetic characteristics of most of these lineages are poorly understood due to limited genome sampling. Here, we addressed 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. Our phylogeny indicated five lineages of zoosporic fungi and placed Blastocladiomycota, which has an alternation of haploid and diploid generations, as branching closer to the Dikarya than to the Chytridiomyceta. Our estimates of heterozygosity based on genome sequence data indicate that the zoosporic lineages plus the Zoopagomycota are frequently characterized by diploid-dominant life cycles. We mapped 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. Together, our results indicate a gradual transition in the genetics and cell biology of fungi from their ancestor and caution against assuming that traits measured in Dikarya are typical of other fungal lineages.
