Relevant Degree Programs
Affiliations to Research Centres, Institutes & Clusters
I would welcome applications from potential graduate students interested in analyzing fossil fungal structures on plant remains from 100 million-year-old Potomac Group strata.
My lab is working towards interpretation of the distinctive Ascomycota fossils preserved on leaf surfaces. Reconstructions of plant/fungal relationships through time are based heavily on molecular phylogenies and molecular dating. This project provides an opportunity to relate fungal fossil diversity to host plants. It will lead to rigorous tests of predictions from molecular phylogenetics about the importance of fungus/plant symbiotic relationships in radiations of terrestrial life.
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Graduate Student Supervision
Doctoral Student Supervision (Jan 2008 - May 2021)
Critical interpretations of fossil fungi combined with phylogenies of living species have the potential to reveal patterns of character evolution and to inform estimates of the geological timing of fungal radiations. Some of the best fungal fossils are of thyriothecia, formed by fly-speck fungi. A thyriothecium is a minute fungal sporulating structure, with a flat scutellum and a shield-like upper surface. Scutella have distinctive cell patterns that are formed by a sequence of hyphal branching and septation. However, for thyriothecial species, phylogenies from DNA sequence data and illustrations of scutella remain have been limited. In Chapter 2, I present a comprehensive phylogeny of thyriothecial Dothideomycetes based on 4251 nucelotides for 320 taxa, contributing new nuclear rDNA sequence data for 14 thyriothecial fungi. I code character states for taxa including 60 thyriothecial species and then estimate ancestral character states using the Bayesian posterior distribution of topologies from my dataset to account for phylogenetic uncertainty. Radiate thyriothecia are only found in Class Dothideomycetes, where they seem to have evolved independently at least three times. In Chapters 3, 4 and 5, I describe new species of Cretaceous scutellum fossils. Scutella can be abundant on fossilized leaf cuticles and are well documented in deposits of Eocene age and younger (
Species delimitation directly affects interpretation of evolution and biogeography. Following speciation, independently evolving lineages are expected to fix different characters that eventually distinguish them from their closest relatives. However, rates of fixation vary. I delimited species in the mushroom genus Russula based on the fungal nuclear internal transcribed spacer 2 (ITS2) DNA barcode region. I sampled 713 ITS2 sequences of American Pacific Northwest specimens collected by Seattle architect Benjamin Woo (1923-2008). I compared the morphology within and among DNA-delimited species, according to morphological character state data that Woo had recorded for each of specimen. To Woo's data, I added spore measurements for 23 species. The characters in Russula varied within and overlapped between my delimited species. My multivariate analysis showed that the centroids of morphological characters usually differed significantly between pairs of genetically defined species, indicating evolutionary divergence at the level of morphology. However, because of the variation among and within conspecific collections, morphological characters only correctly predicted the identity of ~50% of the individual specimens. Of the delimited species, nine had been collected ten or more times each and were, based on morphology and sequence analysis, undescribed and restricted to North America. I describe the nine as new species, reporting their character variation. I used data from public databases to ask how frequently geographical ranges are intercontinental as opposed to intracontinental among mushroom-forming species. I calculated the ‘range extent’ (maximum geographical distance) recorded for 2324 species world-wide and 341 species from the Pacific Northwest, representing 12 genera. The ranges of most species extended only to ~2000 km (shorter distances than a continent). By permutation of the data, I showed that this pattern vanished if geographical coordinates were randomized with respect to species suggesting the pattern I found in the data was not due to random sampling. More sampling would be needed to resolve whether the pattern arose from sampling bias or a high frequency of regional endemism. However, because it reflects a common pattern seen in the best sampled fungi and in narrower studies of genera and families, I hypothesize that regional endemism is the general pattern in well-studied genera and more generally fungal biogeography.
With their threadlike hyphal cells, fungi can invade the surface of a cheese, secreting digestive enzymes and soaking up the spoils. Although most fungi feed with hyphae, phylum Chytridiomycota produces various alternative cell shapes. Here I address three hypotheses regarding the evolution of cell shape. Firstly, Fungi inherited core genes for cellular morphogenesis from their most recent common ancestor and diversification of these genes through evolutionary time potentially contributed to morphological novelty. My phylogenomic surveys revealed duplications in seven families of actin-binding proteins predating the radiation of fungal phyla. Synthesizing previous studies of the function, localization and evolutionary history of septin, myosin, and actin-binding proteins in yeasts and hyphal fungi enabled me to further hypothesize their roles during development in Chytridiomycota. Since Chytridiomycota diverged from moulds and mushrooms, each group evolved unique mechanisms for constructing different cell shapes using a shared ancestral molecular toolkit.Hyphal growth and septation require actin. My second hypothesis was that actin, a major cytoskeletal component, is also involved in morphogenesis in Chytridiomycota. Using fluorescence microscopy, I documented rhodamine phalloidin-stained actin cables, patches, sheets and perinuclear shells through development in Chytriomyces hyalinus. I disrupted the actin cytoskeleton with the chemical inhibitor latrunculin B. Observing actin patches concentrated at rhizoid tips and at cytoplasmic cleavage planes, and finding that actin integrity was essential for rhizoid proliferation in C. hyalinus both support a conserved role for actin in polarized growth and cytokinesis.Thirdly, I hypothesized that sustained tip growth and nuclear migration underlie the convergent evolution of hyphae and hypha-like growth forms. Chytriomyces hyalinus shows determinate growth that ceases once a zoosporangium matures. Phylogenies indicate that filamentous species in Chytridiomycota with indeterminate growth arose independently from ancestors with a determinate growth mode. I determined that actin organization and nuclear migration patterns in each species differed from one another and from hyphae, most likely as a result of their independent origins. In combination, phylogenetic analyses, molecular genetics, and microscopy are tearing away the curtains of time that mask the ever-changing molecular machinery that gave rise to an astounding diversity of form and function in modern fungi.
Precipitated by unexpected discoveries, this thesis is dedicated to the study of the biology of ichthyosporeans. While searching for undiscovered opisthokonts living osmotrophically in marine invertebrate digestive tracts, I established 177 cultures of ichthyosporeans. Ichthyosporeans are one of six understudied unicellular lineages related to the multicellular animals and fungi. Ichthyosporeans are comprised of approximately 30 genera but, prior to this thesis, only four genera had been cultivated. I identified and described three new genera and six species using microscopy and molecular phylogenetic techniques. Two, which I named Abeoforma whisleri and Pirum gemmata, were most closely related to divergent clone sequences and had no known relatives. My other four species, each isolated between eight and 126 times, were related to single isolates Sphaeroforma arctica and Pseudoperkisus tapetis, also found in marine invertebrates. I described one as the new genus and species Creolimax fragrantissima because of its amoeboid reproductive and dispersal stage and fragrance. The other three species were closely related and morphologically indistinguishable. To delimit species, I sequenced three loci from multiple isolates and applied a genealogical concordance species concept. Once delimited, I was able to describe variations in life cycle, morphology and a possible difference in host preference. Rather than adapt cytological techniques to describe the life cycle of S. tapetis, the most abundant species, I used population genetics to work in reverse. Absence of heterozygotes provided evidence for haploidy. Phylogenetic incongruence and a lack of support for linkage between two loci signified a history of recombination consistent with a sexual cycle. I described the ultrastructure of five species using high-pressure frozen cells from healthy, luxuriantly growing cultures. The quality of preservation allowed me to describe features that were new to ichthyosporeans, such as, spindle pole bodies and tubular extensions of the cell that penetrated the cell wall. These features were found in both clades and may have been present in the ancestral ichthyosporean. By combining genetic evidence for sex, observations of asexual reproduction in culture and collection frequencies I proposed a life cycle involving infrequent recombination within a predominantly asexual organism that infected invertebrate hosts indiscriminately via asexual endospores.
Master's Student Supervision (2010 - 2020)
Septins are cytoskeletal proteins important in morphogenesis, cell division and establishing and maintaining cell polarity. Over the course of more than a billion years as Animals and Fungi originated and diversified, their septin genes duplicated and diverged, giving rise to paralogs that encode modular proteins. The septin monomers assemble into heteropolymeric higher order structures that affect cell form by creating physical barriers to diffusion or serving as scaffolds organizing groups of diverse proteins. Here we take advantage of newly sequenced genomes to track the history of septin gene expansions and losses within the phylogeny of Animals and Fungi, including their close protist relatives. By sampling broadly across Opisthokonts, we identified the likely presence of early-diverging animal lineages within Groups 4 and 2A and discovered a novel group of fungal septins not found in Ascomycetes or Basidiomycetes. We hypothesized that previously identified sequence conservation is linked to interface interactions. Using protein homology folding, we mapped interacting residues across Opisthokonts and found that all previously identified motifs were involved in interface interactions, and contained almost all interacting residues. As septin subunit interactions are likely driven by residue identity, we categorized the interacting residues and found specific interface residues associated with each septin Group. We suggest that these residues may explain patterns of septin subunit binding affinity. Notably, we found that Group 3 septins show little conservation within the polybasic region that forms the first alpha helix, found in the NC interface of other septin Groups. This may explain the capping role of Group 3 septins in the yeast septin octamer. With increased sampling, this work identified increased diversity of Opisthokont septins. These proteins show patterns of sequence conservation that are largely driven by conserved interface interactions, in addition to binding of GTP. This work highlights the likely duplications that predate the Opisthokont ancestor, and the structural constraints that shaped the evolution of these multi-purpose septins.Additionally, I attempted to validate and optimize an Agrobacterium-mediated transformation protocol for the chytrid fungus Blastocladiella. While I was unable to conclusively repeat previously published experiments, my work highlighted the difficulties in transformation of these distinct fungi.
Sooty molds from Capnodiaceae are epiphyllous saprotrophs that are often associated with sap-sucking insects. The honeydew exuded by these insects serves as the nutritive substrate for the molds. Through this study I identify an unknown sooty mold on Japanese andromeda, Pieris japonica, from northwestern North America. Morphological analysis of the pycnidial state suggested the fungus is a Fumiglobus species, but with substantial differences from the previously reported species from the genus. In this thesis, I illustrate and describe the epiphyllous mold as Fumiglobus pieridicola. I also provide partial 18S and 28S ribosomal gene sequence data for F. pieridicola. These are the first sequences determined for any species in the genus. Using my sequence dataset, I show that the genus Fumiglobus is within Capnodiaceae with considerable bootstrap support. I also furnish new sequences for the type species of the mitosporic genus Conidiocarpus, also in Capnodiaceae. I confirm that Conidiocarpus is the anamorph of Phragmocapnias. Following the rules of nomenclatural priority, I synonymize Phragmocapnias species under Conidiocarpus. Using ancestral character state reconstruction for Capnodiales, I find a high probability that the ancestor for Capnodiaceae was pycnidial. My analyses contribute to an improved molecular and morphological definition of Capnodiaceae.
Once the ancestors of fungi stopped moving and instead started reaching out with hyphae, their filamentous growth made possible new variety in form and habitat. Hyphae mediated substrate colonization, absorptive nutrition, mating and reproduction. Although shared across most familiar terrestrial fungal lineages, little was known about where hyphae evolved in early fungi. In chapter one, I review the phylogenetic origins of hyphae and current understanding of the cytology of hyphal tips. Better understanding of fungal phylogeny and hyphal growth near the base of the fungal tree was needed. In Chapter 2, I investigated the phylogeny and cytology in the Class Monoblepharidomycetes (Chytridiomycota), a group of deeply diverging, zoosporic fungi, encompassing a range of body types. Species can be either crescent or rod-shaped unicells or sprawling hyphal growths. I inferred a phylogeny of the fungi based on 28S ribosomal DNA sequence data using maximum likelihood (ML) and Bayesian inference methods. I recovered the monophyly of modern fungal phyla and the topology was comparable to the most taxonomically diverse and gene–rich phylogeny of the fungi to date. I used likelihood methods to trace the origins of hyphae on my likelihood tree, concluding that hyphae arose independently in the Monoblepharidomycetes and at least three other times in the fungi. Next, I searched for evidence of convergent evolution in the cellular organization of hyphal Monoblepharidomycetes using fluorescence and transmission electron microscopy. I showed that the hyphae of Monoblepharidomycetes have a novel form with an unusual microtubule cytoskeleton and without a typical fungal Spitzenkörper. This constitutes the first report on the cytology of hyphae from the Chytridiomycota. In Chapter 3, I discuss the significance of my research and possible future directions including cytological experiments on the Monoblepharidomycetes cytoskeleton.
This thesis explores the diversity and phylogenetic structure of the ectomycorrhizal fungal community of western hemlock from five forest types on northern Vancouver Island. Chapter One reviews methods and provides background for studies of ectomycorrhizal fungal communities. In Chapter Two, I describe the results of a new correlative study using recently developed measures of phylogenetic diversity as well as standard measures of diversity and of fungal species composition to relate ectomycorrhizal fungal species to productivity of hemlock trees. I sampled ectomycorrhizal root tips of western hemlock from northern Vancouver Island and amplified, cloned and sequenced the fungal DNA from root extracts. In my analyses, I combined new data from plots of mature western hemlock-amabilis fir stands on Hemlock-Amabilis fir (HA) sites, and from plots of old-growth western red cedar-western hemlock stands on Cedar-Hemlock (CH) sites, with data previously gathered from plots of 24-year-old regenerating hemlock on CH sites. I detected 147 operational taxonomic units among 1435 fungal clone sequences. Phylogenetic diversity indices showed that mature hemlock stands on HA sites had significantly higher ectomycorrhizal fungal diversity than regenerating hemlock stands on CH sites. In an analysis of beta diversity, I found that the species composition of the 24-year-old stands was more similar to the composition of old-growth stands on CH sites than to the species composition of mature stands on HA sites. Fungal species composition was strongly correlated with foliar nitrogen concentration. My phylogenetic analyses of net relatedness of species from forests of different types provided some of the first insights into how ectomycorrhizal fungal communities are structured. I found phylogenetic clustering in the plots of 24-year-old regenerating hemlock stands that contrasted with a pattern of phylogenetic evenness in the plots of mature and old-growth stands. A possible explanation for the difference between the patterns is that the regenerating hemlock stands were selecting for related, r-adapted fungi with similar traits while the older stands had more complex environments and selected for divergent fungi with varied traits. Finally, in Chapter Three I discuss some limitations and strengths of my research study, incorporating ideas on future research and implications.
Recent Tri-Agency Grants
The following is a selection of grants for which the faculty member was principal investigator or co-investigator. Currently, the list only covers Canadian Tri-Agency grants from years 2013/14-2016/17 and excludes grants from any other agencies.
- Tracing the evolution of development among early diverging fungi - Natural Sciences and Engineering Research Council of Canada (NSERC) - Discovery Grants Program - Individual (2016/2017)
- Becoming a fungus: comparative phylogenomic studies of evolution of hyphal growth and absorptive nutrition in fungi - Natural Sciences and Engineering Research Council of Canada (NSERC) - Discovery Grants Program - Individual (2013/2014)
- Diverse organizations of actin and nuclei underpin the evolution of indeterminate growth in chytridiomycota and dikarya (2021)
Botany, 99 (6), 303-320
- Extending the fossil record for foliicolous Dothideomycetes: Bleximothyrium ostiolatum gen. et sp. nov., a unique fly-speck fungus from the Lower Cretaceous of Virginia, USA (2021)
American Journal of Botany, 108 (1), 129-144
- Phylogenetic analysis of the distribution of deadly amatoxins among the little brown mushrooms of the genus Galerina (2021)
PLoS ONE, 16 (2 February)
- A new epiphyllous fly-speck fungus from the Early Cretaceous Potomac Group of Virginia (125–112 Ma): Protographum luttrellii, gen. et sp. nov. (2020)
Mycologia, 112 (3), 504-518
- Character evolution of modern fly-speck fungi and implications for interpreting thyriothecial fossils (2020)
Applications in Plant Sciences, 107 (7), 1021-1040
- Genomic and fossil windows into the secret lives of the most ancient fungi (2020)
Nature Reviews Microbiology
- Actin guides filamentous rhizoid growth and morphogenesis in the zoosporic fungus Chytriomyces hyalinus (2019)
Mycologia, 111 (6), 904-918
- Diversity of opisthokont septin proteins reveals structural constraints and conserved motifs 06 Biological Sciences 0604 Genetics (2019)
BMC Evolutionary Biology, 19 (1)
- Kenneth Wells, 24 July 1927-19 July 2016 (2019)
Mycologia, 111 (3), 525-528
- Over the hills, but how far away? Estimates of mushroom geographic range extents (2019)
Journal of Biogeography, 46 (7), 1547-1557
- New insights into the evolutionary history of fungi from a 407 Ma blastocladiomycota fossil showing a complex hyphal thallus (2018)
Philosophical Transactions of the Royal Society B: Biological Sciences, 373 (1739)
- Early Diverging Fungi: Diversity and Impact at the Dawn of Terrestrial Life (2017)
Annual Review of Microbiology, 71, 41-60
- Fungal diversity notes 603–708: taxonomic and phylogenetic notes on genera and species (2017)
Fungal Diversity, 87 (1)
- Troubles with mycorrhizal mushroom identification where morphological differentiation lags behind barcode sequence divergence (2017)
Taxon, 66 (4), 791-810
- A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data (2016)
Mycologia, 108 (5), 1028-1046
- No place among the living: phylogenetic considerations place the Palaeozoic fossil T. protuberans in Fungi but not in Dikarya. A comment on M. Smith (2016) (2016)
Botanical Journal of the Linnean Society, 182 (4), 723-728
- Phylogenetic evidence places the coralloid jelly fungus Tremellodendropsis tuberosa (Tremellodendropsidales) among early diverging Agaricomycetes (2016)
Mycological Progress, 15 (9), 939-946
- Cytology and molecular phylogenetics of Monoblepharidomycetes provide evidence for multiple independent origins of the hyphal habit in the Fungi (2015)
Mycologia, 107 (4), 710-728
- Online access to the Kalgutkar and Jansonius database of fossil fungi (2015)
Palynology, 39 (1), 103-109
- Phylogenomic analyses indicate that early fungi evolved digesting cell walls of algal ancestors of land plants (2015)
Genome Biology and Evolution, 7 (6), 1590-1601
- Common, unsightly and until now undescribed: Fumiglobus pieridicola sp. nov., a sooty mold infesting Pieris japonica from western North America (2014)
Mycologia, 106 (4), 746-756
- Fungi from PCR to genomics: The spreading revolution in evolutionary biology (2014)
Systematics and Evolution: Part A: Second Edition, 1-18
- Comparative morphology and genealogical delimitation of cryptic species of sympatric isolates of sphaeroforma (Ichthyosporea, Opisthokonta) (2013)
Protist, 164 (2), 287-311
- Phylogenetic structure of ectomycorrhizal fungal communities of western hemlock changes with forest age and stand type (2013)
Mycorrhiza, 23 (6), 473-486
- Cortinarius parkeri, a new species from the Pacific Northwest of North America (2012)
Botany, 90 (4), 327-335
- No jacket required - new fungal lineage defies dress code: Recently described zoosporic fungi lack a cell wall during trophic phase (2012)
BioEssays, 34 (2), 94-102
- A multigene phylogeny of Olpidium and its implications for early fungal evolution (2011)
BMC Evolutionary Biology, 11 (1)
- Cortinarius species diversity in British Columbia and molecular phylogenetic comparison with European specimen sequences (2011)
Botany, 89 (11), 799-810
- Facing Unknowns: Living cultures (Pirum gemmata gen. nov., sp. nov., and Abeoforma whisleri, gen. nov., sp. nov.) from invertebrate digestive tracts represent an undescribed clade within the unicellular opisthokont lineage ichthyosporea (Mesomycetozoea) (2011)
Protist, 162 (1), 33-57
- Dating the molecular clock in fungi - how close are we? (2010)
Fungal Biology Reviews, 24 (1-2), 1-16
- Population-level analyses indirectly reveal cryptic sex and life history traits of pseudoperkinsus tapetis (Ichthyosporea, Opisthokonta): A unicellular relative of the animals (2010)
Molecular Biology and Evolution, 27 (9), 2014-2026
- Transfer of two Helicoma species to Troposporella based on molecular and morphological data (2010)
Mycoscience, 51 (2), 144-148
- Labyrinthulomycetes phylogeny and its implications for the evolutionary loss of chloroplasts and gain of ectoplasmic gliding (2009)
Molecular Phylogenetics and Evolution, 50 (1), 129-140
- Pleospora species with Stemphylium anamorphs: A four locus phylogeny resolves new lineages yet does not distinguish among species in the Pleospora herbarum clade (2009)
Mycologia, 101 (3), 329-339
- The effect of fertilization on the below-ground diversity and community composition of ectomycorrhizal fungi associated with western hemlock (Tsuga heterophylla) (2009)
Mycorrhiza, 19 (4), 267-276
- The Fungi (2009)
Current Biology, 19 (18)
- Multiple Isolations of a Culturable, Motile Ichthyosporean (Mesomycetozoa, Opisthokonta), Creolimax fragrantissima n. gen., n. sp., from Marine Invertebrate Digestive Tracts (2008)
Protist, 159 (3), 415-433
- Preserving accuracy in GenBank (2008)
Science, 319 (5870), 1616
- Rhynie chert: A window into a lost world of complex plant-fungus interactions: Commentary (2007)
New Phytologist, 174 (3), 475-479
- Tubeufia asiana, the teleomorph of Aquaphila albicans in the Tubeufiaceae, Pleosporales, based on cultural and molecular data (2007)
Mycologia, 99 (6), 884-894
- Dating divergences in the Fungal Tree of Life: Review and new analyses (2006)
Mycologia, 98 (6), 838-849
- Molecular phylogeny of Dictyosporium and allied genera inferred from ribosomal DNA (2006)
Fungal Diversity, 21, 157-166
- Molecular systematics of Helicoma, Helicomyces and Helicosporium and their teleomorphs inferred from rDNA sequences (2006)
Mycologia, 98 (1), 94-104
- Phylogenetic relationships and convergence of helicosporous fungi inferred from ribosomal DNA sequences (2006)
Molecular Phylogenetics and Evolution, 39 (3), 587-597
- Systematics and mating systems of two fungal pathogens of opium poppy: The heterothallic Crivellia papaveracea with a Brachycladium penicillatum asexual state and a homothallic species with a Brachycladium papaveris asexual state (2006)
Canadian Journal of Botany, 84 (8), 1304-1326
- Lateral transfer of mating system in Stemphylium (2005)
Proceedings of the National Academy of Sciences of the United States of America, 102 (32), 11390-11395
- Two new Cryptosporiopsis species from roots of ericaceous hosts in western North America (2005)
Studies in Mycology, 53, 53-62
- The phylogenetic position of Spathulospora based on DNA sequences from dried herbarium material (2004)
Mycological Research, 108 (7), 737-748
- Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots (2003)
New Phytologist, 160 (1), 255-272
- Has dual nomenclature for fungi run its course? the article 59 debate (2003)
Mycotaxon, 88, 493-508
- Shared ITS DNA substitutions in isolates of opposite mating type reveal a recombining history for three presumed asexual species in the filamentous ascomycete genus Alternaria (2003)
Mycological Research, 107 (2), 169-182
- Decorospora, a new genus for the marine ascomycete Pleospora gaudefroyi (2002)
Mycologia, 94 (4), 651-659
- Molecular detection, community structure and phylogeny of ericoid mycorrhizal fungi (2002)
Plant and Soil, 244 (1-2), 55-66
- Aliquandostipitaceae, a new family for two new tropical ascomycetes with unusually wide hyphae and dimorphic ascomata (2001)
American Journal of Botany, 88 (1), 52-61
- Lollipopaia minuta from Thailand, a new genus and species of the Diaporthales (Ascomycetes, Fungi) based on morphological and molecular data (2001)
Canadian Journal of Botany, 79 (9), 1099-1106
- Pyrenophora phylogenetics inferred from ITS and glyceradehyde-3-phosphate dehydrogenase gene sequences (2001)
Mycologia, 93 (6), 1048-1063
- The phylogeny of plant and animal pathogens in the Ascomycota (2001)
Physiological and Molecular Plant Pathology, 59 (4), 165-187
- ITS base sequence phylogeny in Bidens (Asteraceae): Evidence for the continental relatives of Hawaiian and Marquesan Bidens (2000)
Systematic Botany, 25 (1), 122-133
- Molecular phylogenetic support from ribosomal DNA sequences for origin of Helminthosporium from Leptosphaeria-like loculoascomycete ancestors (2000)
Mycologia, 92 (4), 736-746
- Ribosomal DNA and resolution of branching order among the Ascomycota: How many nucleotides are enough? (2000)
Molecular Phylogenetics and Evolution, 17 (3), 337-344
- Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences (1999)
Mycologia, 91 (6), 964-977
- Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors (1999)
Proceedings of the National Academy of Sciences of the United States of America, 96 (10), 5592-5597
- Identification of green algal endophytes as the alternate phase of Acrosiphonia (Codiolales, Chlorophyta) using ITS1 and ITS2 ribosomal DNA sequence data (1999)
Journal of Phycology, 35 (3 II), 607-614
- ITS sequences and phylogenetic relationships in Bidens and Coreopsis (Asteraceae) (1999)
Systematic Botany, 24 (3), 480-493
- Molecular diversity of ericoid mycorrhizal fungi (1999)
Canadian Journal of Botany, 77 (11), 1580-1594
- Phylogeny within the genus platismatia based on rDNA its sequences (lichenized ascomycota) (1998)
Cryptogamie: Bryologie et Lichenologie, 19 (4), 307-319
- Loculoascomycete origins and evolution of filamentous ascomycete morphology based on 18S rRNA gene sequence data (1996)
Molecular Biology and Evolution, 13 (3), 462-470
- Phylogenetic origins of the asexual mycorrhizal symbiont Cenococcum geophilum Fr. And other mycorrhizal fungi among the ascomycetes (1996)
Molecular Phylogenetics and Evolution, 6 (2), 287-294
- Is Penicillium monophyletic? An evaluation of phylogeny in the family Trichocomaceae from 18S, 5.8S and ITS ribosomal DNA sequence data (1995)
Mycologia, 87 (2), 210-222
- Dating the evolutionary radiations of the true fungi (1993)
Canadian Journal of Botany, 71 (8), 1114-1127
- Fungal model organisms: Phylogenetics of saccharomyces, aspergillus, and neurospora (1993)
Systematic Biology, 42 (4), 440-457
- Ultrastructural and light microscopic localization of carbohydrates and peroxidase/catalases in Lagenidium giganteum zoospores (1993)
Mycologia, 85 (5), 734-743
- 18S rDNA sequences and the holometabolous insects (1992)
Molecular Phylogenetics and Evolution, 1 (4), 270-278
- 18S Ribosomal RNA gene sequence characters place the human pathogenSporothrix schenckii in the genusOphiostoma (1992)
Experimental Mycology, 16 (1), 87-91
- Convergence in ascospore discharge mechanism among pyrenomycete fungi based on 18S ribosomal RNA gene sequence (1992)
Molecular Phylogenetics and Evolution, 1 (1), 59-71
- Detecting morphological convergence in true fungi, using 18S rRNA gene sequence data (1992)
BioSystems, 28 (1-3), 117-125
- Two ascomycete classes based on fruiting-body characters and ribosomal DNA sequence (1992)
Molecular Biology and Evolution, 9 (2), 278-284
- Yeast biology  (1992)
Science, 257 (5077), 1610-1611
- Specific induction of encystment of Lagenidium giganteum zoospores by concanavalin A and derivatives of chitin and chitosan (1991)
Protoplasma, 161 (1), 43-51