Abstract
The evolutionary history, divergence times and phylogenetic relationships of Uleiella chilensis (Ustilaginomycotina, smut fungi) associated with Araucaria araucana were analysed. DNA sequences from multiple gene regions and morphology were analysed and compared to other members of the Basidiomycota to determine the phylogenetic placement of smut fungi on gymnosperms. Divergence time estimates indicate that the majority of smut fungal orders diversified during the Triassic–Jurassic period. However, the origin and relationships of several orders remain uncertain. The most recent common ancestor between Uleiella chilensis and Violaceomyces palustris has been dated to the Lower Cretaceous. Comparisons of divergence time estimates between smut fungi and host plants lead to the hypothesis that the early Ustilaginomycotina had a saprobic lifestyle. As there are only two extant species of Araucaria in South America, each hosting a unique Uleiella species, we suggest that either coevolution or a host shift followed by allopatric speciation are the most likely explanations for the current geographic restriction of Uleiella and its low diversity. Phylogenetic and age estimation analyses, ecology, the unusual life-cycle and the peculiar combination of septal and haustorial characteristics support Uleiella chilensis as a distinct lineage among the Ustilaginomycotina. Here, we describe a new ustilaginomycetous order, the Uleiellales to accommodate Uleiella. Within the Ustilaginomycetes, Uleiellales are sister taxon to the Violaceomycetales.
Highlights
With more than 1500 known species, smut fungi (Ustilaginomycotina) represent a highly diverse group of plant parasites [1]
Divergence time estimates from the study by Kranitz et al [16] indicated that the stem origin of Araucaria was in the Early Cretaceous to Paleocene (~138–60 mya) and that of the Araucariaceae in the Permian–Triassic (~284–202 mya)
The results of the present study estimated smut fungi to have originated in the Ordovician period (~450 mya), which is in agreement with previous studies [42, 43]
Summary
With more than 1500 known species, smut fungi (Ustilaginomycotina) represent a highly diverse group of plant parasites [1]. Evolution and Phylogeny of Uleiella chilensis doi:10.1371/journal.pone.0147107.g001 yeast-like growth, or with dimorphic life cycles are saprobic [4] or parasitic on animals [5, 6]. The relationship between Uleiella and Araucaria provides a model to explore the origin and evolution of parasitism. Fossils of Araucaria were dated as far back as the Lower Jurassic (~ 200 to 176 mya) [17]. It is unclear (i) whether the parasitic association between Uleiella and Araucaria is the result of co-evolution or a host jump; (ii) whether Uleiella predates its host plant; and (iii) whether Uleiella is ancestral to the smut fungi. Limited ultrastructural data has placed it tentatively in the Ustilaginales [1, 2]
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