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Actin and Ubiquitin Protein Sequences Support a Cercozoan/Foraminiferan Ancestry for the Plasmodiophorid Plant Pathogens

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Actin and Ubiquitin Protein Sequences Support a Cercozoan/Foraminiferan Ancestry for the Plasmodiophorid Plant Pathogens J. Eukaryot. Microbiol., 51(1), 2004 pp. 113±118 q 2004 by the Society of Protozoologists Actin and Ubiquitin Protein Sequences Support a Cercozoan/Foraminiferan Ancestry for the Plasmodiophorid Plant Pathogens JOHN M. ARCHIBALD1 and PATRICK J. KEELING Canadian Institute for Advanced Research, Program in Evolutionary Biology, Department of Botany, University of British Columbia, 3529-6270 University Blvd., Vancouver, British Columbia, V6T 1Z4, Canada ABSTRACT. The plasmodiophorids are a group of eukaryotic intracellular parasites that cause disease in a variety of economically signi®cant crops. Plasmodiophorids have traditionally been considered fungi but have more recently been suggested to be members of the Cercozoa, a morphologically diverse group of amoeboid, ¯agellate, and amoebo¯agellate protists. The recognition that Cercozoa constitute a monophyletic lineage has come from phylogenetic analyses of small subunit ribosomal RNA genes. Protein sequence data have suggested that the closest relatives of Cercozoa are the Foraminifera. To further test a cercozoan origin for the plasmodiophorids, we isolated actin genes from Plasmodiophora brassicae, Sorosphaera veronicae, and Spongospora subterranea, and polyubiquitin gene fragments from P. brassicae and S. subterranea. We also isolated actin genes from the chlorarachniophyte Lotharella globosa. In protein phylogenies of actin, the plasmodiophorid sequences consistently branch with Cercozoa and Foraminifera, and weakly branch as the sister group to the foraminiferans. The plasmodiophorid polyubiquitin sequences contain a single amino acid residue insertion at the functionally important processing point between ubiquitin monomers, the same place in which an otherwise unique insertion exists in the cercozoan and foraminiferan proteins. Taken together, these results indicate that plasmodiophorids are indeed related to Cercozoa and Foraminifera, although the relationships amongst these groups remain unresolved. Key Words. Cercomonads, Cercozoa, chlorarachniophytes, euglyphids, Foraminifera, phylogeny, Plasmodiophora, Plasmodiophorida, Plasmodiophoromycota, polyubiquitin. HE plasmodiophorids are an enigmatic group of obligate Cavalier-Smith and Chao 2003a; Cavalier-Smith and Chao T intracellular parasites, best known as pathogens of eco- 2003b; Van de Peer et al. 2000). The Cercozoa are an extraor- nomically important plants and as vectors for disease-causing dinarily diverse assemblage of ¯agellate, amoebo¯agellate, and plant viruses. The order Plasmodiophorida (informally plas- amoeboid protists that have only recently been recognized as modiophorids) contains 10 genera and 35 species, and includes constituting a monophyletic group through the consideration of Spongospora subterranea, the causative agent of powdery scab molecular data. Included in the Cercozoa are the chlorarach- disease in potato, and Plasmodiophora brassicae, which causes niophytes, the cercomonad ¯agellates, the thaumatomonads, club root disease in cabbage and other Brassicales (Braselton and the euglyphid amoebae (Cavalier-Smith and Chao 2003b). 2000). The most striking feature of plasmodiophorids is their While SSU rRNA phylogenies have been extremely useful possession of a peculiar form of closed mitosis known as cru- in recognizing the Cercozoa as a monophyletic protist lineage, ciform nuclear division, in which a persistent nucleolus elon- they have been less successful at placing these organisms in gates perpendicular to the condensed metaphase chromosomes the global picture of eukaryotic phylogeny (although see Cav- (Braselton, Miller, and Pechak 1975; Dylewski, Braselton, and alier-Smith and Chao 2003a). Signi®cant advances in this area Miller 1978). The group also has several other unusual cell have come from consideration of protein sequence data. Phy- biological characteristics, including the `Rohr and Stachel', a logenetic analyses of the cytoskeletal protein actin have sug- cellular protrusion used by plasmodiophorid zoospores in the gested that Cercozoa are closely related to the Foraminifera infection of host cells (Aist and Williams 1971), and the for- (Keeling 2001), an abundant group of marine and freshwater mation of multinucleate plasmodia inside their hosts (reviewed protists, characterized by the presence of organic or mineralized by Braselton 1995). tests (shells) and granulose pseudopodia (Lee et al. 2002). Sup- A great deal is known about the life cycles, infection strat- port for the idea of a speci®c cercozoan/foraminiferan relation- egies, and basic ultrastructure of plasmodiophorid parasites. ship has been signi®cantly bolstered with the recent discovery However, their highly derived nature has made it dif®cult to of an unusual polyubiquitin gene structure shared between Cer- place these organisms in the context of eukaryotic evolution. cozoa and Foraminifera but absent in all other known eukary- Historically, the plasmodiophorids have been allied with fungi otes (Archibald et al. 2003). Collectively, therefore, actin and (e.g. Waterhouse 1972), due to the fact that they produce spores polyubiquitin are presently two of the best markers with which and have been intensely studied by mycologists from the per- to test a possible relationship with Cercozoa or Foraminifera. spective of plant disease. However, they have also been con- Here we present the ®rst protein sequence data bearing on the sidered protozoa, and the nomenclature for the group has varied question of the evolutionary position of the plasmodiophorids. considerably depending on their presumed phylogenetic af®ni- We sequenced actin and polyubiquitin genes from plasmodi- ties. The recent acquisition of molecular sequence data from ophorids in three different genera. The results support the hy- plasmodiophorids has shed considerable light on their evolu- pothesis that they are related to Cercozoa and Foraminifera. tionary origins. Phylogenetic analyses of small subunit ribo- somal RNA (SSU rRNA) genes have revealed that these or- MATERIALS AND METHODS ganisms are not true fungi (Castlebury and Domier 1998; Ward DNA samples and protist cultures. A sample of Plasmo- and Adams 1998) and have suggested that they belong to the diophora brassicae genomic DNA (gDNA) was kindly provid- protist phylum Cercozoa (formerly Rhizopoda, Bulman et al. ed by Shin-ichi Ito (Yamaguchi University, Japan) and gDNA 2001; Cavalier-Smith 2000; Cavalier-Smith and Chao 1997; samples of Spongospora subterranea and Sorosphaera veroni- cae were provided by Simon R. Bulman (New Zealand Institute for Crop and Food Research, New Zealand) and James P. Bra- Corresponding Author: P. J. KeelingÐTelephone number: 604-822- 4906; FAX number: 604-822-6089; E-mail: pkeeling@interchange. selton (Ohio University, USA). A culture of the chlorarach- ubc.ca niophyte Lotharella globosa (strain CCMP1729) was provided 1 Current address: Department of Biochemistry and Molecular Biol- by Ken-ichiro Ishida (Kanazawa University, Japan) and main- ogy, Dalhousie University, Sir Charles Tupper Medical Building, 5850 tained in f2-Si medium at 20 8C using a 16-h light/ 8-h dark College Street, Halifax, Nova Scotia, B3H 1X5, Canada. cycle. Genomic DNA was extracted from a 100-ml culture of 113 114 J. EUKARYOT. MICROBIOL., VOL. 51, NO. 1, JANUARY±FEBRUARY 2004 L. globosa cells using the DNeasy Plant Mini Kit (Qiagen, San- RESULTS AND DISCUSSION ta Clarita, CA). Plasmodiophorid and chlorarachniophyte actin genes. Ampli®cation, cloning, and sequencing of actin and ubiq- 2 For P. brassicae and L. globosa, three distinct copies of actin uitin genes . Actin coding regions were ampli®ed from the were isolated and two were sequenced from S. veronicae, while gDNAs of P. brassicae, S. subterranea, S. veronicae, and Lo- a single actin gene was ampli®ed from S. subterranea. Within tharella globosa using the following PCR primers: ActF2: 59- a given organism, the different actin gene copies were typically GAGAAGATGACNCARATHATGTTYGA-3 ; ActR1: 5 -GG 9 9 highly similar to one another (sharing . 90% identity), and in CCTGGAARCAYTTNCGRTGNAC-39. Polyubiquitin gene the case of P. brassicae, the actin-1 and actin-2 genes differed fragments were ampli®ed with the following primer pair: only at synonymous (silent) sites. No introns were found in any UBIQ1: 59-GGCCATGCARATHTTYGTNAARAC-39; IUB2: of the plasmodiophorid or L. globosa actin genes determined 5 -GATGCCYTCYTTRTCYTGDATYTT-3 . PCR reactions 9 9 in this study. were performed as follows: after an initial 3-min denaturation Actin phylogeny. The newly obtained P. brassicae, S. sub- at 94 8C, 45 cycles of 45 sec at 92 8C, 1 min at 50 8C, and 1 terranea, and S. veronicae actin sequences form a strongly sup- or 1.5 min at 72 8C were performed. All reactions were ®nished ported monophyletic group in phylogenetic analysis, and the with a ®nal 5-min extension at 72 8C. The UBIQ1/IUB2 primer three L. globosa genes branch with the other chlorarachniophyte set generates a ladder of ubiquitin fragments ranging from a genes characterized in an earlier study (Fig. 1) (Keeling 2001). half-monomer to increasing numbers of the polyubiquitin tract. Together, the plasmodiophorid sequences weakly branch near Ampli®cation products corresponding to 1.5 or 2.5 polyubiqui- the Cercozoa, consistent with the results of SSU rRNA analyses tin repeat units were puri®ed using the UltraCleany 15 DNA (e.g. Bulman et al. 2001; Cavalier-Smith and Chao 1997; Cav- puri®cation kit (MOL BIO Laboratories, Solana Beach, CA), alier-Smith and Chao 2003b). More speci®cally, the plasmodi-
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