| Summary: | <p>Abstract</p> <p>Background</p> <p>From a common ancestor with animals, the earliest fungi inherited flagellated zoospores for dispersal in water. Terrestrial fungi lost all flagellated stages and reproduce instead with nonmotile spores. <it>Olpidium virulentus </it>(= <it>Olpidium brassicae</it>), a unicellular fungus parasitizing vascular plant root cells, seemed anomalous. Although <it>Olpidium </it>produces zoospores, in previous phylogenetic studies it appeared nested among the terrestrial fungi. Its position was based mainly on ribosomal gene sequences and was not strongly supported. Our goal in this study was to use amino acid sequences from four genes to reconstruct the branching order of the early-diverging fungi with particular emphasis on the position of <it>Olpidium</it>.</p> <p>Results</p> <p>We concatenated sequences from the <it>Ef-2</it>, <it>RPB1</it>, <it>RPB2 </it>and <it>actin </it>loci for maximum likelihood and Bayesian analyses. In the resulting trees, <it>Olpidium virulentus</it>, <it>O. bornovanus </it>and non-flagellated terrestrial fungi formed a strongly supported clade. Topology tests rejected monophyly of the <it>Olpidium </it>species with any other clades of flagellated fungi. Placing <it>Olpidium </it>at the base of terrestrial fungi was also rejected. Within the terrestrial fungi, <it>Olpidium </it>formed a monophyletic group with the taxa traditionally classified in the phylum Zygomycota. Within Zygomycota, Mucoromycotina was robustly monophyletic. Although without bootstrap support, Monoblepharidomycetes, a small class of zoosporic fungi, diverged from the basal node in Fungi. The zoosporic phylum Blastocladiomycota appeared as the sister group to the terrestrial fungi plus <it>Olpidium</it>.</p> <p>Conclusions</p> <p>This study provides strong support for <it>Olpidium </it>as the closest living flagellated relative of the terrestrial fungi. Appearing nested among hyphal fungi, <it>Olpidium</it>'s unicellular thallus may have been derived from ancestral hyphae. Early in their evolution, terrestrial hyphal fungi may have reproduced with zoospores.</p>
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