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Phylogenetic Relationships of Plasmopara, Bremia and Other

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Phylogenetic Relationships of Plasmopara, Bremia and Other Mycol. Res. 108 (9): 1011–1024 (September 2004). f The British Mycological Society 1011 DOI: 10.1017/S0953756204000954 Printed in the United Kingdom. Phylogenetic relationships of Plasmopara, Bremia and other genera of downy mildew pathogens with pyriform haustoria based on Bayesian analysis of partial LSU rDNA sequence data Hermann VOGLMAYR1, Alexandra RIETHMU¨LLER2, Markus GO¨KER3, Michael WEISS3 and Franz OBERWINKLER3 1 Institut fu¨r Botanik und Botanischer Garten, Universita¨t Wien, Rennweg 14, A-1030 Wien, Austria. 2 Fachgebiet O¨kologie, Fachbereich Naturwissenschaften, Universita¨t Kassel, Heinrich-Plett-Strasse 40, D-34132 Kassel, Germany. 3 Lehrstuhl fu¨r Spezielle Botanik und Mykologie, Botanisches Institut, Universita¨tTu¨bingen, Auf der Morgenstelle 1, D-72076 Tu¨bingen, Germany. E-mail : [email protected] Received 28 December 2003; accepted 1 July 2004. Bayesian and maximum parsimony phylogenetic analyses of 92 collections of the genera Basidiophora, Bremia, Paraperonospora, Phytophthora and Plasmopara were performed using nuclear large subunit ribosomal DNA sequences containing the D1 and D2 regions. In the Bayesian tree, two main clades were apparent: one clade containing Plasmopara pygmaea s. lat., Pl. sphaerosperma, Basidiophora, Bremia and Paraperonospora, and a clade containing all other Plasmopara species. Plasmopara is shown to be polyphyletic, and Pl. sphaerosperma is transferred to a new genus, Protobremia, for which also the oospore characteristics are described. Within the core Plasmopara clade, all collections originating from the same host family except from Asteraceae and Geraniaceae formed monophyletic clades; however, higher-level phylogenetic relationships lack significant branch support. A sister group relationship of Pl. sphaerosperma with Bremia lactucae is highly supported. Within Bremia lactucae s. l., three distinct clades are evident, which only partly conform to the published host specificity groups. All species of the genera Basidiophora, Bremia, Paraperonospora and Plasmopara included in the present study were investigated for haustorial morphology, and all had ellipsoid to pyriform haustoria, which are regarded as a diagnostic synapomorphy of the whole clade. Aspects of coevolution and cospeciation within the downy mildew pathogens with ellipsoid to pyriform haustoria are briefly discussed. INTRODUCTION (Constantinescu & Fatehi 2002, Riethmu¨ ller et al. 2002, Go¨ ker et al. 2003). Haustorial morphology may be one Until recently, hypotheses on phylogenetic relation- such feature. Already in the extensive investigation of ships of downy mildew pathogens were mainly based Fraymouth (1956), morphology of haustoria was shown on morphological criteria (e.g. Shaw 1981, Dick to be characteristic for some groups, e.g. the large et al. 1989). These hypotheses suffered from both the globose to lobate haustoria of the Peronospora species paucity of distinct morphological features and a poor now classified in Hyaloperonospora (Constantinescu & understanding of the majority of taxa which are not Fatehi 2002, Go¨ ker et al. 2003). On the other hand, economically important plant pathogens. However, Fraymouth (1956) argued that ‘_ the form and struc- molecular phylogenetics opened a new era, and much ture of hyphae and haustoria does not offer help in progress has been gained in the re-evaluation of classification _’, which may be partly explained by the relationships within Peronosporales (Riethmu¨ ller et al. obsolete downy mildew classification on which she 2002, Go¨ ker et al. 2003). based her considerations. Riethmu¨ ller et al. (2002) demonstrated that In the course of their molecular and morphological morphological features (e.g. conidiosporangiophore studies, Constantinescu & Fatehi (2002), Riethmu¨ ller morphology) used in traditional classification were et al. (2002) and Go¨ ker et al. (2003) re-evaluated haus- sometimes overemphasized or incorrectly interpreted. torial morphology of downy mildew pathogens with a However, such studies also revealed the phylogenetic new phylogenetic background. The genera Hyaloper- significance of other previously underestimated features onospora (Constantinescu & Fatehi 2002) and Viennotia Phylogeny of Plasmopara and related genera 1012 ellipsoid-pyriform hyphal clavate-branched Pseudoperonospora Plasmopara Bremia lactucae core Paraperonospora unknown/absent Basidiophora Plasmopara pygmaea Peronospora sparsa Phytophthora infestans Phytophthora arecae agg. Peronophythora litchii Sclerospora Pythium monospermum Viennotia Pythium undulatum hyphal Hyaloperonospora Peronospora large globose-lobate core 20 µm hyphal-branched Fig. 1. Simplified phylogenetic tree based on Go¨ ker et al. (2003: fig. 1), with a presentation of the different haustorial types of downy mildew genera. Several taxa of the core Peronospora clade have been pruned from the original tree for a better graphic presentation. Branches in bold denote presumed apomorphic haustorial types. Hyphal haustoria are interpreted as a plesiomorphic character, as they are also present in some species of Phytophthora. Although basically hyphal (Fraymouth 1956), the haustoria of Pseudoperonospora are here recognised as distinct due to their characteristic clavate- branched (‘digitate’) shape. All drawings to the same scale and from the generic type species, except for Plasmopara (from Pl. umbelliferarum); haustoria of Viennotia redrawn from Go¨ ker et al. (2003), all others original drawings. (Go¨ ker et al. 2003) were segregated from the genera The genera with ellipsoid to pyriform haustoria Peronospora and Plasmopara, respectively, partly based (Basidiophora, Bremia, Paraperonospora and Plasmo- on differences in haustorial morphology. On the basis para) have been shown to be closely related and form a of this information, two haustorial types can be sup- monophyletic entity within the Peronosporales (Rieth- posed to be apomorphic for monophyla: large globose mu¨ ller et al. 2002, Go¨ ker et al. 2003). As comparatively to lobate haustoria for the Hyaloperonospora clade, few taxa were included in former studies, extended sam- and ellipsoid to pyriform haustoria for a clade pling of these genera was initiated to examine whether containing Basidiophora, Bremia, Paraperonospora this pattern was consistent over a wider range of taxa. and Plasmopara. The clavate-branched haustoria of The present study is a further step towards a more Pseudoperonospora are basically hyphal, but could be natural delimitation and classification of the genera of interpreted as apomorphic. On the other hand, the downy mildew pathogens, and it demonstrates that hyphal haustoria of Peronospora, Sclerospora and many taxa are still in need of thorough morphological Viennotia can be regarded as plesiomorphic, as this and molecular investigation. In addition, the present type has also been found in the genus Phytophthora study addresses species delimitation in Bremia and (e.g. Phytophthora infestans; Erwin & Ribeiro 1996). Plasmopara, a problem still largely unresolved. However, data on haustoria in Phytophthora are in- sufficient to draw far-reaching conclusions, and further phylogenetic and morphological investigations are MATERIALS AND METHODS necessary. A summary of the current information on Sample sources, DNA-extraction, PCR and sequencing molecular phylogeny and haustorial types is shown in Fig. 1; the data on haustorial morphology are based The organisms contained in the study are listed in on own, extensive original observations. Table 1. For Phytophthora, the nomenclature of H. Voglmayr and others Table 1. Collection data and GenBank accession numbers of the taxa studied. The taxa are grouped taxonomically; the ordinal classification follows Kirk et al. (2001) and Dick (2001), respectively. Collectors: AR, A. Riethmu¨ ller; FO, F. Oberwinkler; HV, H. Voglmayr; KH, L. Kisimova-Horovitz; MG, M. Go¨ ker; MM, M. Mennicken; MP, M. Piepenbring; RK, R. Kirschner. Vouchers: LPB; La Paz (Bolivia); TUB, University of Tu¨ bingen; WU, University of Vienna. Collection data GenBank Taxon Isolated from/host Origin/source (voucher) accession no. Peronosporales Basidiophora entospora Conyza canadensis Austria: Lower Austria, Langenlois, HV (WU), HV123 AY035513 B. entospora C. canadensis France: Dept. Ain, near Bourg en Bresse, HV & AR (TUB), F8 AY250145 Bremia lactucae Arctium sp. Austria: Lower Austria, Merkersdorf, HV (WU), AR388 AY250120 B. lactucae Carduus nutans Austria: Vienna, HV (WU), HV232 AY250126 B. lactucae C. personata Austria: Tirol, Umbaltal, HV (WU), HV653 AY250124 B. lactucae Carlina acaulis Austria: Carinthia, Großfragant, HV (WU), HV482 AY250117 B. lactucae Centaurea cyanus Austria: Lower Austria, Theresienfeld, HV (WU), HV197h AY250123 B. lactucae C. jacea Austria: Upper Austria, St Willibald, HV (WU), HV526 AY250119 B. lactucae C. cf jacea Germany: Baden-Wu¨ ttemberg, Onstmettingen, HV & AR (TUB), AR264 AY250118 B. lactucae C. montana Germany: Bavaria, Oberjoch, HV (WU), HV586 AY250132 B. lactucae C. cf pullata France: Dept. He´ rault, SW Montpellier, between Se` te and Agde, HV & AR (WU), F31 AY250121 B. lactucae Cirsium acaule Austria: Tirol, near Weißenbach, MG (TUB), MG1836, MG3 AY250122 B. lactucae C. arvense Austria: Upper Austria, St Willibald, HV (WU), HV778 AY250125 B. lactucae C. oleraceum Austria: Upper Austria, St Willibald, HV (WU), HV704 AY035507 B. lactucae C. vulgare Germany: Baden-Wu¨ ttemberg, Tu¨ bingen-Lustnau, HV (WU), HV835 AY250131 B. lactucae Crepis sancta France: Dept. Droˆ me, S Lyon, W Romans s/Ise`
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