On the Evolutionary History of Uleiella chilensis, a Smut Fungus Parasite of Araucaria araucana in South America: Uleiellales ord. nov. in Ustilaginomycetes

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.

针对与智利南洋杉（Araucaria araucana）共生的智利油杉黑粉菌（Uleiella chilensis，隶属于黑粉菌亚门（Ustilaginomycotina））的演化历史、分化时间及系统发育关系展开了分析。研究对多基因区域的DNA序列与形态学特征进行分析，并与担子菌门（Basidiomycota）的其他类群进行比对，以明确寄生裸子植物的黑粉菌的系统发育定位。分化时间估算结果显示，绝大多数黑粉菌目类群的分化发生于三叠纪-侏罗纪时期，但部分类群的起源与系统发育关系仍未明确。智利油杉黑粉菌与沼泽紫丝膜菌（Violaceomyces palustris）的最近共同祖先可追溯至早白垩世。通过对比黑粉菌与寄主植物的分化时间估算结果，我们提出假说：早期黑粉菌亚门类群具有腐生生活方式。目前南美仅存两种智利南洋杉属物种，各自宿主均拥有专属的油杉黑粉菌（Uleiella）物种，据此我们认为，协同进化或寄主转移后伴随异域成种，是当前油杉黑粉菌属地理分布受限且物种多样性较低的最合理解释。系统发育与年龄估算分析、生态学特征、异常的生活史，以及隔膜与吸器特征的独特组合，均支持智利油杉黑粉菌作为黑粉菌亚门中一个独立演化支的结论。本研究描述了一个新的黑粉菌纲（Ustilaginomycetes）目——油杉黑粉菌目（Uleiellales），以容纳油杉黑粉菌属类群。在黑粉菌纲中，油杉黑粉菌目与紫膜菌目（Violaceomycetales）互为姊妹群。