Implications of molecular characters for the phylogeny of the Microbotryaceae (Basidiomycota: Urediniomycetes)

BMC Evolutionary Biology BioMed Central Research article Open Access Implications of molecular characters for the phylogeny of the Microbotryaceae (Basidiomycota: Urediniomycetes) Martin Kemler*†, Markus Göker†, Franz Oberwinkler and Dominik Begerow Address: Lehrstuhl für Spezielle Botanik und Mykologie, Botanisches Institut, Universität Tübingen, Auf der Morgenstelle 1, D-72076 Tübingen, Germany Email: Martin Kemler* - ; Markus Göker - ; Franz Oberwinkler - ; Dominik Begerow - * Corresponding author †Equal contributors Published: 25 April 2006 BMC Evolutionary Biology 2006, 6:35 doi:10.1186/1471-2148-6-35 Received: 07 November 2005 Accepted: 25 April 2006 This article is available from: http://www.biomedcentral.com/1471-2148/6/35 © 2006 Kemler et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Anther smuts of the basidiomycetous genus Microbotryum on Caryophyllaceae are important model organisms for many biological disciplines. Members of Microbotryum are most commonly found parasitizing the anthers of host plants in the family Caryophyllaceae, however they can also be found on the anthers of members of the Dipsacaceae, Lamiaceae, Lentibulariaceae, and Portulacaceae. Additionally, some members of Microbotryum can be found infecting other organs of mainly Polygonaceae hosts. Based on ITS nrDNA sequences of members of almost all genera in Microbotryaceae, this study aims to resolve the phylogeny of the anther smuts and their relationship to the other members of the family of plant parasites. A multiple analysis strategy was used to correct for the effects of different equally possible ITS sequence alignments on the phylogenetic outcome, which appears to have been neglected in previous studies. Results: The genera of Microbotryaceae were not clearly resolved, but alignment-independent moderate bootstrap support was achieved for a clade containing the majority of the Microbotryum species. The anther parasites appeared in two different well-supported lineages whose interrelationship remained unresolved. Whereas bootstrap support values for some clades were highly vulnerable to alignment conditions, other clades were more robustly supported. The differences in support between the different alignments were much larger than between the phylogenetic optimality criteria applied (maximum parsimony and maximum likelihood). Conclusion: The study confirmed, based on a larger dataset than previous work, that the anther smuts on Caryophyllaceae are monophyletic and that there exists a native North American group that diverged from the European clade before the radiation of the European species. Also a second group of anther smuts was revealed, containing parasites on Dipsacaceae, Lamiaceae, and Lentibulariaceae. At least the majority of the parasites of Asteraceae appeared as a monophylum, but delimitations of some species in this group should be reconsidered. Parasitism on Polygonaceae is likely to be the ancestral state for the Microbotryaceae on Eudicot hosts. Background The genera of Microbotryaceae Anther smuts of the genus Microbotryum that parasitise members of the Caryophyllaceae are well-established Page 1 of 15 (page number not for citation purposes) BMC Evolutionary Biology 2006, 6:35 model organisms. They have been subject to research in different areas, i.e. genetics (e.g. [1]), population analysis (e.g. [2]), phylogenetics (e.g. [3]), host-parasite evolution [4], and ecology [5]. The sorus formation of smuts in the anthers of the hosts is an interesting constellation that has been discussed in the context of pollination. Lateral transmission of the parasite by the pollinator is thought to have a significant effect on the evolutionary history of the genus and its distribution on different hosts [5]. There are ten recognized species of caryophyllaceous anther smuts [6,7], but the species concept in this group is discussed quite controversially. Some authors define at least some species as formae speciales of Microbotryum violaceum (Pers.) G. Deml & Oberw. [3,8-10]. In contrast, Liro [11], based on infection experiments and field observations, already separated Ustilago violacea (Pers.) Roussel (i.e. Microbotryum violaceum) into several species. Molecular studies also indicate genetical isolation of lineages parasitising different host plants [7,10] or occurring in different geographical regions [3]. Against this background, it is desirable to further our understanding of this group. Furthermore, it is noteworthy that the caryophyllaceous anther smuts are only a minor group in Microbotryum. On the basis of ultrastructural features, the Microbotryaceae are defined as phytoparasitic Basidiomycota that have transversely septate basidia with multiple production of sessile basidiospores and intercellular hyphae but no haustoria [12]. The Microbotryaceae are separated from their sister family, the Ustilentylomataceae, by having hyphae with poreless septa at maturity [12]. For an extensive historical overview of Microbotryum see [6]. Vánky [6] revised Microbotryum, and, based on spore mass colour, transferred most of the Ustilago species that parasitise eudicotyledonous plants to Microbotryum. Later, new species were added [7,13,14], and Microbotryum now contains 77 species. Even though the caryophyllaceous anther smuts are the best-known members of the genus, most species are parasites on Polygonaceae. Hosts are also described in the Asteraceae, Dipsacaceae, Gentianaceae, Lamiaceae, Lentibulariaceae, and Onagraceae. The formation of sori is not restricted to anthers, but there is sorus formation in seeds, whole flowers, pedicels, stems, and leaves. Next to Microbotryum the Microbotryaceae contain Bauerago Vánky, Liroa Cif., Sphacelotheca de Bary, and Zundeliomyces Vánky [15]. So far, no hypotheses have been formulated about how these genera might be related to each other. Sphacelotheca is distinct from Microbotryum by forming appendices between spores, the so-called disjunctors, and by the presence of a columella and a peridium in the sori [16,17]. Liroa forms tumours on its host plants including an apical lunular bed of spore masses [16-19]. Bauerago is characterized by its parasitism on Cyperaceae http://www.biomedcentral.com/1471-2148/6/35 and Juncaceae, the presence of a peridium and the lack of a columella [20]. In order to obtain hypotheses about the phylogenetic relationships of the main groups in the Microbotryaceae, we performed molecular phylogenetic analyses based on nuclear internal transcribed spacer (ITS) sequences. Besides Microbotryum, specimens of Bauerago, Liroa, and Sphacelotheca were included in our analyses. Thus, with the exception of the monotypic genus Zundeliomyc (...truncated)