Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109.
School of Biology and Ecology, University of Maine, Orono, ME 04473.
Proc Natl Acad Sci U S A. 2022 Sep 6;119(36):e2116841119. doi: 10.1073/pnas.2116841119. Epub 2022 Aug 29.
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.
真菌界的大多数描述物种都包含在两个门中，子囊菌门和担子菌门（后鞭毛亚界）。因此，我们对该界生物学的理解受到后鞭毛亚界中观察到的特征的严重影响，例如气生孢子的扩散以及以单倍体核有丝分裂为主的生命周期。我们现在意识到，真菌除了后鞭毛亚界之外，还包含许多门级谱系，但由于基因组采样有限，这些谱系中的大多数的系统发育和遗传特征都知之甚少。在这里，我们通过对真真菌的游动孢子（鞭毛）谱系的 69 个新生成的草图基因组序列的系统基因组分析，研究了非后鞭毛真菌的主要进化趋势。我们的系统发育表明，游动孢子真菌有五个谱系，并将具有单倍体和二倍体世代交替的芽枝菌门放置在与后鞭毛亚界比与壶菌门更为接近的分支位置。我们基于基因组序列数据的杂合度估计表明，游动孢子谱系加上Zoopagomycota 通常以二倍体为主的生命周期为特征。我们在系统发育上绘制了其他特征，例如祖先细胞周期调节剂、细胞膜和细胞壁相关基因，以及氨基酸硒代半胱氨酸的使用，并发现这些与Metazoa 共享的祖先特征在游动孢子谱系中已经广泛发生了平行缺失。总的来说，我们的结果表明真菌的遗传学和细胞生物学从其祖先开始逐渐转变，并提醒人们不要假设在后鞭毛亚界中测量的特征是其他真菌谱系的典型特征。
