| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Mycology and Plant Pathology |
2Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 USA; 3USDA-ARS, Cereal Disease Laboratory and the Department of Plant Pathology, University of Minnesota, St. Paul,Minnesota 55108 USA
Received for publication September 11, 2003. Accepted for publication January 22, 2004.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: Agaricostilbum pulcherrimum • cytoskeleton • evolution • immunofluorescence • microtubules • nuclear small subunit rDNA • Urediniomycetes
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Mueller et al., 1998
; Suh et al., 2003
). Although generally considered ascomycetes, yeasts are widely distributed in all three classes of Basidiomycota (Fell et al., 2001
), including the homobasidiomycetes (Mueller et al., 1998
). Because their simplicity yields few structural characters, most data used to classify yeasts are molecular or physiological. As reviewed by McLaughlin et al. (1995)
, microscopic analyses of fungal cells have provided informative phylogenetic characters, such as spindle pole body form, nuclear division features, and cytoplasmic organization. Therefore, we have been exploring the mitotic and cytoskeletal patterns of basidiomycetous yeasts (Frieders and McLaughlin, 1996
; McLaughlin et al., 1996
) as a source of additional phylogenetic characters.
During budding in the yeast cell cycle, the products of mitosis are distributed between the parent and bud. Changes in the cytoskeleton and the positions of the nucleus and spindle are revealed more easily through immunofluorescence localization of microtubules and DNA than through traditional ultrastructural analyses. Two general mitotic patterns have been found to distinguish ascomycetous and basidiomycetous budding yeasts (McLaughlin et al., 1996
). In ascomycetous yeasts, nuclear migration is associated with a discrete bundle of microtubules originating at the spindle pole body; spindle initiation and early elongation occur in the parent; and nuclear elongation proceeds from the parent into the bud (Kilmartin and Adams, 1984
; Barton and Gull, 1988
). In most basidiomycetous yeasts, nuclear migration is associated with a basket of cortical microtubules; spindle initiation and early elongation occur in the bud; and nuclear elongation proceeds from the bud back into the parent (Frieders and McLaughlin, 1996
; McLaughlin et al., 1996
).
Of the budding basidiomycetous yeasts studied cytologically, the majority are classified within the Urediniomycetes (Swann et al., 2001
). Only three basidiomycetous yeasts were studied previously with immunofluorescence (Frieders and McLaughlin, 1996
; McLaughlin et al., 1996
), and these three taxa are placed within the three major clades of this class. Kriegeria eriophori and Septobasidium carestianum both share the common basidiomycetous yeast mitotic pattern (McLaughlin et al., 1996
). Agaricostilbum pulcherrimum, however, possesses characters intermediate between those of ascomycetes and basidiomycetes (Frieders and McLaughlin, 1996
). It is not clear whether what occurs in A. pulcherrimum is unique within Basidiomycota and whether this species retains an ancestral division pattern.
To address these uncertainties, we identified yeast species within the Agaricostilbomycetidae (as described by Swann et al., 2001
) through a molecular analysis of a range of urediniomycetous taxa. Two taxa, Stilbum vulgare and Bensingtonia yuccicola, were chosen based on their degree of relatedness to A. pulcherrimum. The monotypic, dimorphic S. vulgare produces a minute stipitate sporocarp with a spherical head, bearing two-celled basidia; each cell produces one basidiospore, suggesting binucleate basidiospores. Basidiospores germinate to form the yeast stage. This organism is widely distributed on a variety of substrates, such as angiosperm wood and bark, weathered and dead inflorescences, and mushrooms; it has been reported from Europe, North America, and Australia (Seifert et al., 1992
). Bensingtonia yuccicola is a mitosporic yeast that produces ballistoconidia. It was reported from a dead fallen yucca leaf in Vancouver, British Columbia, Canada (Nakase and Suzuki, 1988
).
In the following report, we present a molecular phylogeny for representatives of the Agaricostilbomycetidae of the Urediniomycetes and elucidate the mitotic and cytoskeletal patterns in the yeast phase of S. vulgare and B. yuccicola. The results are compared to those from A. pulcherrimum and other yeasts, and their phylogenetic relevance is discussed.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
.
DNA was extracted using the method of Lee and Taylor (1990)
and was amplified and purified as described in Swann et al. (1999)
. Sequences were obtained by cycle sequencing using fluorochrome-labeled dideoxynucleotides (ABI sequencing apparatus, Molecular Genetics Instrumentation Facility, University of Georgia, Athens, Georgia, USA). DNA sequence data were assembled and checked for accuracy by comparing forward and reverse strands. DNA sequences were aligned using the program CLUSTAL W (Thompson et al., 1994
) and the multiple sequence editor in MacVector (version 7.0, Genetics Computer Group, Madison, Wisconsin, USA). DNA sequence alignment and trees have been submitted to TreeBASE (www.treebase.org): study accession number S1071, matrix accession number M1827.
Unweighted and weighted phylogenetic analyses were performed using PAUP* version 4.0b10 (Swofford, 2003
). Of 1843 characters, 493 were parsimony informative. Twenty-seven characters (190–199, 240–242, 679–685, 782–785, 1554–1556) were removed from the analysis, three sequence regions were eliminated because of questionable alignment, and two unique insertions in Mixia were reduced to single characters. Parsimony trees were obtained using a heuristic search, stepwise addition, random addition sequence, 10 replicates. Bootstrap support was determined with a full heuristic search, 1000 replicates. Base change frequencies were determined for the two parsimony trees using unambiguous changes in MacClade version 4.0 (Maddison and Maddison, 2000). Less frequent base changes were weighted more heavily than more frequent changes. Weights were determined as in Swann et al. (1999)
.
Cultures and cell preparation
Bensingtonia yuccicola strain ML 3193 (CBS 7331) was obtained from Jack Fell (Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, Key Biscayne, Florida, USA), and Stilbum vulgare strain RJB 75–9295-B was obtained from R. J. Bandoni (Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada). Cultures were maintained on malt yeast peptone (MYP) agar (Bandoni and Johri, 1972
) and incubated at 21°C under fluorescent light under a 16-h light:8-h dark cycle.
A modification of the method of Taylor and Wells (1979)
was used to synchronize budding to maximize the number of dividing cells. Twenty-four-hour-old cultures were used to inoculate new MYP plates, 0.75 mL of sterile distilled water was added, and yeasts were spread with a sterilized bent glass rod. For Bensingtonia yuccicola, budding was synchronized at 16 h and for S. vulgare, at 24 h.
Freeze-substitution and immunofluorescent labeling
Freezing, fixation, and immunolabeling procedures followed those outlined in Frieders and McLaughlin (1996)
and McLaughlin et al. (1996)
, with slight modifications. Following collection on Mylar, plunge-freezing, and freeze-substitution in methanolic formaldehyde (3.7%), the cells were warmed gradually to room temperature. Cells were postfixed in a solution of 90% methanolic formaldehyde and 10% phosphate buffer containing 0.1 mol/L magnesium sulfate and 0.1 mol/L EGTA (both added to stabilize microtubules), followed by a secondary postfixation in 85% methanolic formaldehyde plus 1% glutaraldehyde in the same buffer. Yeast cells were rehydrated in an increasing buffer series. Some cells were released from the Mylar at each rehydration step; these cells were collected by centrifugation and rehydrated separately from those cells still attached to Mylar, until all cells were collected. Wall digestion, membrane permeabilization, and blocking reactions and subsequent rinses used phosphate-buffered saline with 0.1 mol/L magnesium sulfate and 0.1 mol/L EGTA.
Immunolocalization was performed using monoclonal antialpha-tubulin YOL1/34 (Amersham, Little Chalfont, UK) diluted 1:100 in buffered 1% bovine serum albumin. The secondary antibody was fluorescein isothiocyanate (FITC)-conjugated antirat IgG. Following labeling and staining with 4,6-diamidino-2-phenylindole dihydrochloride (DAPI), cells were mounted in Tris-HCl and 1,4-diazobicyclo(2,2,2)-octane in glycerol. Prepared slides were viewed with a Zeiss Axioskop using a Neofluor 100x/1.3 NA objective with an Optovar setting of 1.25x or 1.6x, barrier filters appropriate for FITC and DAPI observation, and differential interference contrast (DIC) optics. Photographs were taken using Kodak T-Max 400 ISO film at ISO 1600 (Kodak, Rochester, New York, USA).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
Bensingtonia yuccicola mitosis
Cells of Bensingtonia yuccicola (Figs. 2–26) were generally ovoid in shape; however, some cells were nearly spherical, with buds forming from the parent in an apical to subapical position in all cells studied. All parent cells and most cells without buds contained a vacuole of varying size, clearly seen in DIC images (Figs. 4, 7, 10, 13, 16, 19, 22, 25). Occasionally, the vacuole interfered with the microtubule image (Fig. 20) but did not affect its interpretation.
|
|
At metaphase (Figs. 8–16, 26c, 26d), spindles were located in the bud oriented approximately parallel to the long axis of the bud. Bud size was variable and not closely correlated with the spindle length. Early in metaphase, most of the chromatin was located in the bud associated with the spindle, but some chromatin remained in the parent (Figs. 9, 12). It became entirely located within the bud as metaphase proceeded (Fig. 15). Spindle initiation was not observed. At early metaphase (Figs. 8–10, 26c), spindles were short and lacked astral microtubules. Later in metaphase (Figs. 11–16, 26d), the spindle elongated minimally, the chromatin became fully condensed, and short asters were observed.
The spindle began its major elongation during anaphase (Figs. 17–19, 26e), with a concomitant separation of chromatin. One spindle pole and the associated chromatin extended back into the parent. Astral microtubules became more pronounced at each pole. At telophase (Figs. 20–22, 26f), remnants of broken spindles were observed. Both asters reached their greatest development, extending to the cell periphery. Nuclei remained condensed at the spindle poles. At post-mitotic interphase (Figs. 23–25, 26g), asters disappeared and the cortical microtubule cytoskeleton gradually reformed in a pattern similar to that seen in late interphase (Fig. 2). Daughter nuclei enlarged and appeared in random positions in both the parent and bud. Nucleoli reformed at this stage.
Stilbum vulgare mitosis
Cells of Stilbum vulgare (Figs. 27–60) were ovoid and budded apically. Almost all cells of this species were binucleate, but a few uninucleate cells were observed (not illustrated). Vacuoles were smaller than those in B. yuccicola and did not interfere with microtubule observation. Non-budding interphase cells were common, and the nuclei stained readily, but the microtubule cytoskeleton could not be localized despite many attempts (see upper cell in Figs. 54– 56). With bud initiation, microtubule localization became possible (Fig. 27).
|
|
The two nuclei in each cell proceeded through mitosis asynchronously, and the spindles often were oriented at different angles. While the two mitotic apparatuses could be viewed clearly and interpreted via through-focusing, this clarity was not apparent in the two-dimensional photographic images.
Spindle initiation occurred in the parent (Fig. 30, arrow); early spindle elongation occurred primarily in the parent (Figs. 30, 33, 36) and rarely in the parent–bud junction (Fig. 33, arrow). During prometaphase (Figs. 30–32, 60b), the localized microtubules formed around the spindle pole body and appeared as a small bilobed dot associated with the condensing chromatin. At early metaphase (Figs. 30–35, 60b), the spindle elongated somewhat and was oriented perpendicular to the long axis of the cell. Chromatin was somewhat more condensed. Nuclei no longer were located distally in the parent and varied from a central to proximal position in the parent. As metaphase proceeded (Figs. 36–41, 60c), spindles were oriented obliquely or nearly parallel to the long axis of the cell. Short and sparse astral microtubules appeared, and chromatin became progressively more condensed until it resembled a metaphase plate. At meta-anaphase (Figs. 42–44) the asters became somewhat more pronounced and the chromatin began to move toward the poles.
In anaphase (Figs. 45–53, 60d, 60e), the spindle elongated completely, chromatin separated and reached the spindle poles, and astral microtubules developed fully. The proximal spindle poles and associated chromatin entered the bud one at a time, doing so at different anaphase stages, sometimes entering at early anaphase (Figs. 45–47, upper arrow), mid-anaphase (Fig. 48, lower arrow), or at late anaphase (Figs. 51–53, upper arrowhead). In early to mid-anaphase (Figs. 45, 48), there was limited spindle elongation, the distal spindle poles remained relatively stationary, while the proximal poles moved toward and sometimes through the parent–bud junction. The spindle elongated greatly during late anaphase (Figs. 51–53, 60e). By mid-anaphase (Figs. 49, 60d), the daughter chromatin separated fully and reached the poles. As anaphase proceeded, astral microtubules reached their maximum length, extending to or nearly to the cell periphery (Fig. 48).
In telophase (Figs. 51–56, 60e, 60f), spindles were fully elongated, extending from the apex of the bud to the distal end of the parent. By late telophase, spindles were broken and partially disassembled (Fig. 54). Astral microtubules were short, forming a minute fan at the poles. The forming daughter nuclei, located at the cell extremities, were still condensed (Fig. 55). In postmitotic interphase (Figs. 57–59, 60g), long, randomly oriented, cortical cytoskeletal microtubules were present. Nuclei were fully decondensed and medianly positioned, and nucleoli appeared (Fig. 58).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
, which used partial nuclear large subunit gene and ITS regions, and we obtained much higher bootstrap support values. These results place Chionosphaera in the Agaricostilbomycetidae, as do other studies on this subclass (Swann et al., 1999
, 2001
; Fell et al., 2001
; Scorzetti et al., 2002
), and establish it as a sibling taxon to Stilbum vulgare. Based on structural characters, S. vulgare has been classified within the Chionosphaeraceae (Oberwinkler and Bauer, 1989
), and molecular evidence supports this placement. Although S. vulgare was included in the Atractiellales (Oberwinkler and Bandoni, 1982
), our study further confirms its removal from this order (Oberwinkler and Bauer, 1989
).
Previous studies of mitosis using immunofluorescence methods in three genera of basidiomycetous yeasts, each in a different subclass of Urediniomycetes (Frieders and McLaughlin, 1996
; McLaughlin et al., 1996
), have demonstrated that the typical mitotic pattern involves nuclear division in the bud rather than the parent and are in agreement with ultrastructural studies of basidiomycetes in general (McCully and Robinow, 1972a
, b
; Poon and Day, 1976a
, b
; Taylor and Wells, 1979
; Boekhout and Linnemans, 1982
; Mochizuki et al., 1987
). The present study focused on three genera in a single subclass and shows that mitotic studies using immunofluorescence localizations have phylogenetic significance. Agaricostilbum pulcherrimum (Frieders and McLaughlin, 1996
) and Stilbum vulgare have cystoskeletal and mitotic characters suggestive of an intermediate position between ascomycetes and basidiomycetes. In both species, spindle initiation and early elongation occur in the parent, as in ascomycetes (Kilmartin and Adams, 1984
; Barton and Gull, 1988
; Danková et al., 1988
); early in mitosis, nuclear migration toward the bud is associated with a cortical basket of microtubules and late in mitosis, the spindle in the bud elongates back into the parent, as in other basidiomycetes (Frieders and McLaughlin, 1996
; McLaughlin et al., 1996
). The mitotic pattern in budding cells of Bensingtonia yuccicola follows that of typical basidiomycetes with spindle initiation originating in the bud. If common equals primitive, then these results can be interpreted as indicating that the ascomycetous pattern in A. pulcherrimum and S. vulgare is derived rather than basal. Also, these two taxa are gasteroid, a condition known to be derived multiple times within Basidiomycota. Correctly interpreting character evolution, however, requires molecular phylogenies from multiple genes presently being pursued through the Assembling the Fungal Tree of Life project (http://ocid.NACSE.ORG/research/ aftol/), because the deep roots for basidiomycetes, as for fungi in general, are unknown.
In dimorphic basidiomycetes, production of dikaryotic asexual propagules is common, although these generally arise from the dikaryotic mycelium rather than from the yeast stage (Bandoni, 1995
). Seifert et al. (1992)
reported the yeast stage of S. vulgare to be haploid. Although some monokaryotic yeast cells were found during our investigations of S. vulgare, the vast majority were binucleate and regenerated via a standard budding method. The tremellaceous Trimorphomyces papilionaceus also has a dikaryotic yeast stage, but its method of regeneration differs from that of S. vulgare yeasts in that the parent cell produces two haploid conidia that fuse and enlarge to become a dikaryotic yeast cell (Oberwinkler and Bandoni, 1983
). Less than 1% of known yeasts have been studied using these immunofluorescence cytological techniques. Of those studied, S. vulgare is the only dikaryotic species examined. The dikaryotic yeast stage of S. vulgare is unusual and may be a by-product of its two-celled basidium. It is unclear whether the binucleate condition influences the site of mitosis. In A. pulcherrimum the uninucleate yeast stage also initiates mitosis in the parent. There is no obvious reason why the binucleate condition would require initiation of nuclear division in the parent. To address the apparent uniqueness of the mitotic pattern in S. vulgare, how widespread the dikaryotic condition is among basidiomycetous yeasts would have to be determined.
To date five genera of basidiomycetous yeasts have been studied with immunofluorescence methods, and the phylogenetic utility of cytoskeletal and mitotic characters is supported. Based on these limited studies, there appear to be major mitotic differences between ascomycetous and basidiomycetous yeasts. Characters that unite the basidiomycetes thus far are the cortical basket of microtubules early in mitosis associated with nuclear migration toward the bud, and spindle elongation from the bud back into the parent. As in basidiomycetes, yeasts are scattered through all major ascomycete clades (Kurtzman and Sugiyama, 2001
). The mitotic patterns of even fewer ascomycetous, than basidiomycetous, yeasts have been analyzed, and these studies are not representative of ascomycetous yeast taxonomic diversity. We anticipate that further cytological studies of yeasts in both phyla will yield additional characters of phylogenetic value.
|
FOOTNOTES |
|---|
The authors thank Robert Bandoni and Jack Fell for cultures, Susan Wick for advice on immunofluorescence methods, Maiko Papke and Jennifer Alt for contributions to the research, and Bryn Dentinger for assistance. Supported by National Science Foundation grants DEB-9306578, DEB-9318232, and DEB-0228671.
Mention of a trademark name or proprietary product does not constitute a guarantee by the U.S. Department of Agriculture. This article is in the public domain and not copyrightable. It may be freely reprinted with customary crediting of the source. 
5 Present address: Department of Biology, University of Wisconsin-Platteville, Platteville, WI 53818
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Bandoni R. J. B. N. Johri 1972 Tilletiaria: a new genus in the Ustilaginales. Canadian Journal of Botany 50: 39-43
Barnes S. M. D. J. Lane M. L. Sogin C. Bibeau W. G. Weisburg 1991 Evolutionary relationships among pathogenic Candida species and relatives. Journal of Bacteriology 173: 2250-2255
Barton R. K. Gull 1988 Variation in cytoplasmic microtubule organization and spindle length between the two forms of the dimorphic fungus Candida albicans. Journal of Cell Science 91: 211-220
Berbee M. L. J. W. Taylor 1993 Dating the evolutionary radiations of the true fungi. Canadian Journal of Botany 71: 1114-1127[ISI]
Boekhout T. W. A. M. Linnemans 1982 Ultrastructure of mitosis in Rhodosporidium toruloides. Studies in Mycology 22: 23-38
Bowman B. H. J. W. Taylor A. G. Brownlee J. Lee S. D. Lu T. J. White 1992 Molecular evolution of the fungi: relationships of the Basidiomycetes, Ascomycetes, and Chytridiomycetes. Molecular Biology and Evolution 9: 285-296[Abstract]
Danková R. R. J. Hasek E. Streblová 1988 Tubulin and actin patterns in the cell cycle of Saccharomycodes ludwigii Hansen. Canadian Journal of Microbiology 34: 1310-1315[ISI]
De Wachter R. J. M. Neefs A. Goris V. Van De Peer 1992 The gene coding for small ribosomal subunit RNA in the basidiomycete Ustilago maydis contains a group I intron. Nucleic Acids Research 20: 1251-1257
Fell J. W. T. Boekhout A. Fonseca J. P. Sampaio 2001 Basidiomycetous yeasts. In D. J. McLaughlin, E. G. McLaughlin, and P. A. Lemke [eds.], The Mycota, vol. 7B, 3–35. Springer-Verlag, Berlin, Germany
Frieders E. M. D. J. McLaughlin 1996 Mitosis in the yeast phase of Agaricostilbum pulcherrimum and its evolutionary significance. Canadian Journal of Botany 74: 1392-1406[ISI]
Hamamoto M. T. Nakase 2000 Phylogenetic analysis of the ballistoconidium-forming yeast genus Sporobolomyces based on 18S rDNA sequences. International Journal of Systematic and Evolutionary Microbiology 50: 1373-1380[Abstract]
Kilmartin J. V. A. E. M. Adams 1984 Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. Journal of Cell Biology 98: 922-933
Kurtzman C. P. J. W. Fell [eds.] 1998 The yeasts, a taxonomic study. Elsevier, Amsterdam, The Netherlands
Kurtzman C. P. C. J. Robnett 2003 Phylogenetic relationships among yeasts of the ‘Saccharomyces complex’ determined from multigene sequence analyses. FEMS Yeast Research 3: 417-432[CrossRef][ISI][Medline]
Kurtzman C. P. J. Sugiyama 2001 Ascomycetous yeasts and yeastlike taxa. In D. J. McLaughlin, E. G. McLaughlin, and P. A. Lemke [eds.], The Mycota, vol. 7A, 179–200. Springer-Verlag, Berlin, Germany
Lee S. B. J. W. Taylor 1990 Isolation of DNA from fungal mycelia and single spores. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White [eds.], PCR protocols, 282–287. Academic Press, San Diego, California, USA
Maddison D. R. W. P. Maddison 2000 MacClade 4: analysis of phylogeny and character evolution. Version 4.0. Sinauer, Sunderland, Massachusetts, USA
McCully E. K. C. F. Robinow 1972a Mitosis in heterobasidiomycetous yeasts. I. Leucosporidium scottii (Candida scottii). Journal of Cell Science 10: 857-881
McCully E. K. C. F. Robinow 1972b Mitosis in heterobasidiomycetous yeasts. II. Rhodosporidium sp. (Rhodotorula glutinis) and Aessosporon salmonicolor (Sporobolomyces salmonicolor). Journal of Cell Science 11: 1-31
McLaughlin D. J. E. M. Frieders M. E. Berres J. C. Doublés S. M. Wick 1996 Immunofluorescence analysis of the microtubule cytoskeleton in the yeast phase of the basidiomycetes Kriegeria eriophori and Septobasidium carestianum. Mycologia 88: 339-349[CrossRef][ISI]
McLaughlin D. J. E. M. Frieders H. S. Lü 1995 A microscopist's view of heterobasidiomycete phylogeny. Studies in Mycology 38: 91-109
Mochizuki T. S. Tanaka S. Watanabe 1987 Ultrastructure of the mitotic apparatus in Cryptococcus neoformans. Journal of Medical and Veterinary Mycology 25: 223-233
Mueller U. G. S. A. Rehner T. R. Schultz 1998 The evolution of agriculture in ants. Science 281: 2034-2038
Nakase T. M. Suzuki 1988 Sporobolomyces yuccicola, a new species of ballistosporous yeast equipped with ubiquinone-9. Antonie van Leeuwenhoek 54: 47-55[CrossRef][ISI][Medline]
Nishida H. K. Ando Y. Ando A. Hirata J. Sugiyama 1995 Mixia osmundae: transfer from the Ascomycota to the Basidiomycota based on evidence from molecules and morphology. Canadian Journal of Botany 73: 660-666
Oberwinkler F. R. J. Bandoni 1982 A taxonomic survey of the gasteroid, auricularioid Heterobasidiomycetes. Canadian Journal of Botany 60: 1726-1750[ISI]
Oberwinkler F. R. J. Bandoni 1983 Trimorphomyces: a new genus in the Tremellaceae. Systematic and Applied Microbiology 4: 105-113
Oberwinkler F. R. Bauer 1989 The systematics of gasteroid, auricularoid Heterobasidiomycetes. Sydowia 41: 224-256
Poon N. H. A. W. Day 1976a Somatic nuclear division in the sporidia of Ustilago violacea. III. Ultrastructural observations. Canadian Journal of Microbiology 22: 495-506[ISI][Medline]
Poon N. H. A. W. Day 1976b Somatic nuclear division in the sporidia of Ustilago violacea. IV. Microtubules and the spindle pole body. Canadian Journal of Microbiology 22: 507-522[ISI][Medline]
Scorzetti G. J. W. Fell A. Fonseca A. Statzell-Tallman 2002 Systematics of basidiomycetous yeasts: a comparison of large subunit D1/D2 and internal transcribed spacer rDNA regions. FEMS Yeast Research 2: 495-517[ISI][Medline]
Seifert K. A. F. Oberwinkler R. Bandoni 1992 Notes on Stilbum vulgare and Fibulostilbum phylacicola gen. et sp. nov. (Atractiellales). Boletin de la Sociedad Argentina de Botanica 28: 213-217
Sogin M. L. K. Miotto L. Miller 1986 Primary structure of the Neurospora crassa small subunit ribosomal RNA coding region. Nucleic Acids Research 14: 9540
Sugiyama J. T. Inamura G. Okada W. Sjamsuridzal H. Kawasaki A. Hirata 1995 Divergence and molecular evolution among basidiomycetous yeasts with the tropical and subtropical genus Graphiola. Progress in microbial ecology: proceedings of seventh international symposium on microbial ecology, Santos, San Paulo, Brazil, 173–180
Suh S.-O. J. McHugh M. Blackwell 2003 One to 42 taxa: expansion of the Candida tanzawaensis yeast clade from basidiocarpic feeding beetles. Inoculum 54: 47 (Abstract)
Suh S.-O. J. Sugiyama 1993 Phylogeny among the basidiomycetous yeasts inferred from small subunit ribosomal DNA sequence. Journal of General Microbiology 139: 1595-1598[Medline]
Suh S.-O. J. Sugiyama 1994 Phylogenetic placement of the basidiomycetous yeasts Kondoa malvinella and Rhodosporidium dacryoidium, and the anamorphic yeast Sympodiomycopsis paphiopedili by means of 18S rRNA gene sequence analysis. Mycoscience 35: 367-375[CrossRef]
Swann E. C. E. M. Frieders D. J. McLaughlin 1999 Microbotryum, Kriegeria and the changing paradigm in basidiomycete classification. Mycologia 91: 51-66
Swann E. C. E. M. Frieders D. J. McLaughlin 2001 Urediniomycetes. In D. J. McLaughlin, E. G. McLaughlin, and P. A. Lemke [eds.], The Mycota, vol. 7B, 37–56. Springer-Verlag, Berlin, Germany
Swann E. C. J. W. Taylor 1995 Phylogenetic diversity of yeast-producing basidiomycetes. Mycological Research 99: 1205-1210[ISI]
Swofford D. L. 2003 PAUP*: phylogenetic analysis using parsimony (* and other methods), version 4. Sinauer Associates, Sunderland, Massachusetts, USA
Taylor J. W. K. Wells 1979 A light and electron microscopic study of mitosis in Bullera alba and the histochemistry of some cytoplasmic substances. Protoplasma 98: 31-62[CrossRef][ISI]
Thompson J. D. D. G. Higgins T. J. Gibson 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acid Research 22: 4673-4680
This article has been cited by other articles:
|
|
 |
|
  M. C. Aime, P. B. Matheny, D. A. Henk, E. M. Frieders, R. H. Nilsson, M. Piepenbring, D. J. McLaughlin, L. J. Szabo, D. Begerow, J. P. Sampaio, et al. An overview of the higher level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences Mycologia, November 1, 2006; 98(6): 896 - 905. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Lutzoni, F. Kauff, C. J. Cox, D. McLaughlin, G. Celio, B. Dentinger, M. Padamsee, D. Hibbett, T. Y. James, E. Baloch, et al. Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits Am. J. Botany, October 1, 2004; 91(10): 1446 - 1480. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
