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A <I>COX2</I> Molecular Phylogeny of the Peronosporomycetes

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A <I>COX2</I> Molecular Phylogeny of the Peronosporomycetes University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of 2000 A COX2 Molecular Phylogeny of the Peronosporomycetes Deborah S.S. Hudspeth Northern Illinos University Steven A. Nadler University of California - Davis, [email protected] Michael E.S. Hudspeth Northern Illinois University, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/parasitologyfacpubs Part of the Parasitology Commons Hudspeth, Deborah S.S.; Nadler, Steven A.; and Hudspeth, Michael E.S., "A COX2 Molecular Phylogeny of the Peronosporomycetes" (2000). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 743. https://digitalcommons.unl.edu/parasitologyfacpubs/743 This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Copyright 2000, Mycological Society of America. Used by permission. Mycologia, 92(4), 2000, pp. 674-684. ( 2000 by The Mycological Society of America, Lawrence, KS 66044-8897 A COX2 molecular phylogeny of the Peronosporomycetes Deborah S. S. Hudspeth reflected by the inclusion of the autotrophic heter- Department of Biological Sciences, Northern Illinois okont chromophytic algae (chlorophylls a and c); the University,DeKalb, Illinois 60115 heterotrophic unicellular slopalinids (Proteromonas; et al bicosoecids et al Steven A. Nadler Leipe 1996), (Cafeteria; Leipe 1994) and Developayella (Leipe et al 1996); and ad- Department of University of California, Nematology, ditional heterotrophic fungus-like heterokont groups Davis, California 95616 such as the thraustochytrids, labyrinthulids and hy- Michael E. S. Hudspeth' phochytriomycetes. Despite the apparent extreme di- Department of Biological Sciences, Northern Illinois versity of its members the monophyly of the strami- University,DeKalb, Illinois 60115 nipiles has been strongly supported by several molec- ular systematic studies using data derived from small subunit r-RNA (SSURNA) and/or large subunit r- Abstract: The evolutionary history of the mitochon- RNA (e.g., Forster et al 1990, Leipe et al 1994, Van drial COX2 locus has been used to infer the phylo- de Peer et al 1996, Van der Auwera et al 1995) and genetic relationships among 15 peronosporomycete actin (Bhattacharya et al 1991, Bhattacharya and and a hyphochytriomycete species. This molecular Ehlting 1995) gene sequences. phylogenetic analysis at both the ordinal and generic The Peronosporomycetes are a ubiquitous group levels provides strong evidence for the recognition of of over 65 recognized genera (500-800 described the Saprolegniomycetidae and the Peronosporomy- species) with representatives found in most moist cetidae as natural and for the groups, monophyly of habitats (Dick 1990, 1995). The primary economic the Saprolegniales, Leptomitales and Pythiales. A impact of the Peronosporomycetes results from the three amino acid event insertion/deletion (indel) phytopathogenic genera, which include as hosts a has been identified as a for putative synapomorphy wide variety of leguminous and cereal crops, and for- the of 12 mor- Saprolegniales. Parsimony mapping est and rosaceous fruit trees. As the causative agents and biochemical characters on the COX2 phological of downy mildews, white rusts, and a variety of root molecular yields an hypothesis for peron- phylogeny rots and late blights they are a significant detriment osporomycete ancestral states and shared-derived fea- to agriculture. Similarly, infection of roe, fingerlings, tures. or freshwater and marine crustaceans and molluscans Key Words: Achlya, Aphanomyces, Apodachlya, cy- is of increasing concern to the rapidly expanding tochrome c oxidase, Dictyuchus, Hyphochytrium,La- field of aquaculture. Yet despite their economic im- genidium, Leptolegnia, Leptomitus, Oomycetes, Peron- pact, no formal cladistic analysis involving more than ophythora, Peronosporomycetidae, Phytophthora, Plec- a few peronosporomycetes is available, and the evo- tospira, Pythiopsis, Pythium, Saprolegnia, Saprolegni- the diverse Thraustotheca lutionary relationships among genera omycetidae, within the class remain unresolved. Over the last 25 yr the major taxa of the Peronos- poromycetes have undergone significant revision. INTRODUCTION The most traditional organization placed the taxa in four orders: the The Peronosporomycetes, traditionally referred to as major Saprolegniales (Dick 1973a), the the oomycetes, are a class of fungus-like heterotrophs Leptomitales (Dick 1973b), Lagenidiales and the placed in the Kingdom Straminipila (for initial as- (Sparrow 1973), Peronosporales (Water- house Several reassessments of semblage see Patterson 1989). The diversity of this 1973). major peron- Kingdom, whose sole synapomorphy is the appear- osporomycete systematics followed (e.g., Cavalier- ance of tripartite tubular hairs (stramenopiles) at Smith 1981, 1986, 1987, Beakes 1987) with the most some point during the life cycle of its members, is detailed reorganizations proposed by Dick et al (1984) and Dick (1990, 1995). In generating the Accepted for publication January 13, 2000. most recent of these taxonomic revisions Dick (1995) 1 Email: [email protected] has provided a testable set of relationships. Based pri- 674 HUDSPETHET AL: PERONOSPOROMYCETE PHYLOGENY 675 marily on overall similarities of morphological char- rather than eufungal mitochondrial polypeptides. acters, three subclasses (Peronosporomycetidae, Sap- More recently Paquin et al (1995) and Chesnick et rolegniomycetidae, and Rhipidiomycetidae) were al (1996) used P infestans amino acid data (NDH5 erected with requisite subdivision and redistribution and NDH4L) to infer a noneufungal straminipilous of existing orders. relationship for the Peronosporomycetes. Given the paucity of morphological and biochem- In this study we have constructed an hypothesis for ical data for inferring peronosporomycete relation- the evolutionary history of the peronosporomycete ships, molecular-based approaches are very promis- mitochondrial locus (COX2) encoding subunit 2 ing for understanding peronosporomycete phyloge- (COII) of cytochrome c oxidase. By extension, DNA ny. Unfortunately, published molecular phylogenetic and deduced amino acid sequence data from 15 per- studies have typically included only one to five gen- onosporomycete taxa and a hyphochytriomycete era, and were primarily intended to assess the rela- have been used to infer the phylogenetic relation- tionships of peronosporomycetes to other major eu- ships among peronosporomycete species. Specifically, karyotic groups. One of those studies (Forster et al we ask if there is molecular support for the recogni- 1990) used three SSURNA sequences to represent tion of the Saprolegniomycetidae and the Peronos- the Peronosporomycetidae and Saprolegniomyceti- poromycetidae as natural groups; and, whether there dae; these authors noted that the three sequences is support for the placement of the Leptomitales were very similar to each other and suggested that within the Saprolegniomycetidae as recently pro- less conserved DNA sequences may be needed. Sub- posed (Dick 1995). The analyses presented here rep- sequently, Lee and Taylor (1992) inferred relation- resent the first rigorous cladistic analysis of this eco- ships among several Phytophthoraspecies using more nomically important, but greatly understudied class variable rDNA internal transcribed spacer sequences. of the Straminipila. Neither of these studies, however, was intended to infer a peronosporomycete phylogeny per se, nor has MATERIALSAND METHODS a formal cladistic analysis of this group been pub- lished to date. Based on these reports and other stud- Strains and media.-Straminipile taxa used in this study ies where SSURNA data were sometimes unable to were obtained from the followingsources (ATCCcatalogue resolve closely related taxa (e.g., Nadler and Hud- numbersin parentheses):Achlya ambisexualis E87 (11400), speth 1998), we examined alternative loci prior to A. Barksdale,New YorkBotanical Garden, New York,New initiating our molecular phylogenetic analysis of the York;Aphanomyces euteiches A466 S.E. Holub, Universityof Wisconsin,Madison, lacteus Peronosporomycetes. Wisconsin;Leptomitus (38076), J. Aronson,Arizona State University,Tempe, Arizona;Pyth- Several factors suggested that the use of mtDNA ium ultimum67-1 (32939),J.G. Hancock,University of Cal- would be in a helpful establishing peronosporomy- ifornia, Berkeley,California; Saprolegnia ferax (36051), I.B. cete Foremost these the ex- phylogeny. among were: Heath, YorkUniversity, Toronto, Ontario, Canada.Dictyu- tensive physical (Hudspeth et al 1983, Klimczak and chus sterilis(44891), Hyphochytriumcatenoides (18719), La- Prell 1984, McNabb et al 1987, McNabb and Klassen genidiumgiganteum (36492), Leptolegniacaudata (48818), 1988, Shumard-Hudspeth and Hudspeth 1990) and Peronophythoralitchii (28739), Plectospira myriandra genic (Shumard et al 1986, Shumard-Hudspeth and (64139), Pythiopsiscymosa (26880), Thraustothecaclavata Hudspeth 1990, Hudspeth 1992, Hudspeth and Hud- (34112) were all purchaseddirectly from ATCC,Manassas, speth 1996) characterizations of a wide variety of per- Virginia.Apodachlya pyrifera
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