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Phylogeny of the Ophiostoma stenoceras–Sporothrix schenckii complex

     Department of Microbiology & Plant Pathology, Forestry & Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0001 South Africa

Thomas C. Harrington

     Department of Plant Pathology, Iowa State University, Ames, Iowa 50010

Hester F. Vismer

     Programme on Mycotoxins & Experimental Carcinogenesis (PROMEC), Medical Research Council, P.O. Box 19070, Tygerberg, 7505 South Africa

Brenda D. Wingfield

     Department of Genetics, Forestry & Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0001 South Africa

Michael J. Wingfield

     Forestry & Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0001 South Africa

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

Ophiostoma stenoceras is a well-known sapwood-colonizing fungus occurring on some coniferous and hardwood hosts in the Northern Hemisphere. In the Southern Hemisphere, the fungus has been reported only from New Zealand. The human pathogen, Sporothrix schenckii, has been suggested to be the anamorph of O. stenoceras. The aim of this study was to gain a better understanding of the phylogenetic relationship between these two species. The study also provided the opportunity to confirm the identity of some Sporothrix and O. stenoceras-like isolates recently collected from wood and soil around the world. For this purpose, the DNA sequence of internal transcribed spacer (ITS) regions of the ribosomal RNA operon was determined. Isolates of O. nigrocarpum, O. albidum, O. abietinum, O. narcissi and O. ponderosae, all morphologically similar to O. stenoceras, were included in the study. From phylogenetic analyses of the sequence data, four main clades were observed. These represented O. stenoceras, O. nigrocarpum and two separate groups containing isolates of S. schenckii. Our results confirm earlier suggestions that S. schenckii should be classified within the teleomorph genus Ophiostoma but support studies separating O. stenoceras and S. schenckii. Ophiostoma albidum and O. ponderosae should be considered synonyms of O. stenoceras. The status of O. narcissi and O. abietinum needs further clarification. The two groups within S. schenckii might represent two species, but this needs to be confirmed. This study represents the first reports of O. stenoceras from Colombia, Kenya, Uruguay and South Africa.

Key words: abietinum, albidum, ITS, narcissi, nigrocarpum, ponderosae, rDNA

	INTRODUCTION

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Ophiostoma stenoceras (Robak) Nannf. is a sapwood-colonizing fungus that first was described from ground wood pulp in Norway (Robak 1932). It since has been isolated from many other coniferous hosts, as well as some hardwood trees from the Northern Hemisphere (Davidson 1942, Griffin 1968, Otani 1988). In the Southern Hemisphere, O. stenoceras has been reported only from New Zealand (Farrell et al 1997, Schirp et al 1999). The fungus causes a slight gray stain on pine and spruce (Kåårik 1980) but is not considered economically important (Davidson 1942, Griffin 1968).

The first suggestion that O. stenoceras might represent the teleomorph of Sporothrix schenckii Hektoen & Perkins, the causative agent of human sporotrichosis, was made by Mariat (Mariat et al 1968, Mariat 1971a, b, Nicot and Mariat 1973). The relationship between O. stenoceras and S. schenckii since has been the subject of many research papers. A wide variety of taxonomic criteria were employed in these studies; they included conidium morphology, vitamin requirements, starch degradation, resistance to digestion by macrophage cells, immunological studies, cell wall components, neutral and polar lipid composition, carbohydrate composition, acid phosphatase isoenzyme patterns and pathogenicity studies (De Hoog 1974, Travassos and Lloyd 1980, Summerbell et al 1993). Molecular investigations included techniques such as DNA-DNA hybridisation, GC content (Mendonça-Hagler et al 1974) and mitochondrial restriction fragments (Suzuki et al 1988). The results of these studies often were contradictory, some suggesting that S. schenckii was the anamorph of O. stenoceras (Taylor 1970, De Hoog 1974) and others showing differences between the two species (Mendonça-Hagler et al 1974, Travassos et al 1974, Suzuki et al 1988). All these investigations were reviewed by Travassos and Lloyd (1980), as well as by Summerbell et al (1993). Although Travassos and Lloyd concluded that S. schenckii "bears little relation" to O. stenoceras, and a list of suggested criteria to distinguish between the two species was compiled (Summerbell et al 1993), the phylogenetic relationship between the two fungi never was clarified.

Berbee and Taylor (1992) confirmed with DNA sequencing that S. schenckii is phylogenetically related to Ophiostoma. The 18S rDNA gene sequenced in their study is highly conserved and does not exhibit sufficient variability to allow for distinction between closely related species. The aim of our study, therefore, was to gain a better understanding of the phylogenetic relationships between O. stenoceras and S. schenckii. To achieve this goal, we sequenced both the internal transcribed spacer (ITS) regions, including the 5.8S rRNA gene, of the ribosomal RNA operon. Isolates of Ophiostoma spp. that are morphologically similar to O. stenoceras also were included in the study. These were O. nigrocarpum (Davidson) De Hoog, O. albidum Mathiesen-Kåårik, O. abietinum Marmolejo & Butin, O. narcissi Limber and O. ponderosae (Hinds & Davidson) Hausner, Reid & Klassen. The study also provided us with the opportunity to confirm the identity of some Sporothrix and O. stenoceras-like isolates from wood and soil that recently have been collected from various Southern Hemisphere countries.

	MATERIALS AND METHODS

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Isolates – Isolates resembling O. stenoceras and O. nigrocarpum (Table I ) were collected from wood, bark beetles and soil from various countries, worldwide. Authenticated isolates of both these species, as well as one isolate each of O. abietinum, O. albidum, O. narcissi and O. ponderosae, were obtained from the Centraalbureau voor Schimmelcultures (CBS), Utrecht, Netherlands, the American Type Culture Collection (ATCC), Manassas, Virginia, U.S.A., and the CABI Bioscience Genetic Resource Collection (IMI), Surrey, United Kingdom. The isolates of O. abietinum (C696) and O. ponderosae (C87) are associated with the types of the respective species, as is the O. stenoceras isolate CMW3202. The O. albidum isolate (C1190) was one of the isolates examined by Mathiesen-Kåårik (1953) when she described the species. Unfortunately no type material was designated for the species (Hunt 1956), and no culture representing type material exists.

Where isolations were made from wood samples, these were initially incubated in Petri dishes with moist tissue paper at room temperature. After the appearance of either perithecia or conidiophores, spore masses were transferred from these structures to 2% Biolab malt-extract agar (MEA), and the cultures were purified.

For isolations from soil, 1 g of each sample was diluted in 100 mL sterile water. A dilution series with five dilutions was made. Of each of the dilutions, 1 mL was plated onto 2% malt- and 0.2% yeast-extract agar (MYA). The plates were incubated at 20 C for 1–3 d. Colonies with a Sporothrix-like appearance were transferred to clean MEA plates and purified. Isolates from bark beetles and humans were obtained following the methods described by Hsiau and Harrington (1997) and Vismer and Hull (1997), respectively.

O. ulmi (Buisman) Nannf. and O. ips (Rumbold) Nannf. isolates included as outgroups in the phylogenetic analysis have been sequenced as part of an earlier study (Harrington et al 2001).

All isolates in this study are maintained on MEA slants at 4 C in either the culture collection (CMW) of the Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa, or in the culture collection (C) of T. C. Harrington, Department of Plant Pathology, Iowa State University, U.S.A. (Table I).

DNA sequencing and sequence analysis – To conduct phylogenetic analyses, isolates were grown 10 d in a liquid medium containing 2% malt extract. DNA was extracted using the method of DeScenzo and Harrington (1994). A part of the ribosomal DNA operon, including the 3' end of the small subunit (SSU) rDNA gene, internal transcribed spacer (ITS) region 1, the 5.8S rRNA gene, ITS region 2 and the 5' end of the 26S large subunit rDNA gene (LSU), was amplified using PCR with the primers ITS1-F (Gardes and Bruns 1993) and ITS4 (White et al 1990). The reaction mixture (50 µL final volume) contained 2.6 U Expand^TM High Fidelity Taq Polymerase mixture (Boehringer Mannheim, South Africa), 5 µL PCR reaction buffer, 3 mM MgCl₂, 0.2 mM of each dNTP, and 0.2 mM of each primer. PCR reactions were performed in a Hybaid Touchdown PCR machine (Hybaid, Middlesex, UK). PCR conditions were: one cycle of 2 min at 95 C, followed by 40 cycles of 30 s at 95 C, 30 s at 55 C and 1 min at 72 C, followed by one cycle of 8 min at 72 C. PCR products were visualized by electrophoresis on a 1% (w/v) agarose gel, stained with ethidium bromide.

PCR fragments were purified using the QIAquick PCR purification kit. Both strands of the PCR fragments were sequenced using the primers ITS1-F, ITS4, CS2 and CS3 (Wingfield et al 1996) and the Thermo Sequenase Dye Terminator Cycle Sequencing Premix Kit (Amersham Life Science). Sequences were determined with an ABI Prism 377 Automatic DNA sequencer (Perkin Elmer).

The nucleotide sequences were aligned manually and the phylogenetic analyses performed using PAUP (phylogenetic analysis using parsimony) 4.0b2a (Swofford 1998). Uninformative characters were excluded and a heuristic search, using TBR (Tree Bisection and Reconstruction) branch swapping (MULPAR on), was conducted to determine the most-parsimonious trees. Trees were rooted with sequences of O. ulmi and O. ips. One thousand bootstrap analyses were run to determine confidence levels at the branching points. Aligned data and tree were deposited at TreeBASE (Study accession number = S788; Matrix accession number = M1248).

	RESULTS

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Sequence analysis – PCR products of the isolates of ingroup species were approximately 530 bp in size. Within the ITS 1 region of all isolates, there was a GC rich area of approximately 70 bp. This area proved difficult to sequence, probably due to GC folding, resulting in secondary structures that would be difficult for the polymerase to read through. S. schenckii isolates proved to be the most difficult to sequence. Although it was possible to get the full sequence for most of the isolates, there were five isolates for which approximately 25 bases could not be determined. Manual alignment of the dataset resulted in a total of 617 characters, including gaps. From the GC rich area in ITS 1, 61 characters were excluded from the analyses. Of the remaining 556 unordered characters, 353 were constant, 89 variable characters were parsimony uninformative, leaving 114 informative characters in the analyses. Most of the variation in the sequence data was found within the ITS 1 region.

Using O. ulmi and O. ips as outgroup taxa, 80 most-parsimonious trees (CI = 0.828, HI = 0.172, RI = 0.937) of 308 steps were produced. Four main clades were resolved in all trees. Variation among the trees resulted from minor branch alternatives within the main clades. A single tree was chosen for presentation (Fig. 1). Bootstrap values supporting the branches of groups O. stenoceras and O. nigrocarpum were 100% and 90% respectively. The two clades of the S. schenckii complex each were supported with 100% confidence.

View larger version (23K): [in this window] [in a new window]   FIG. 1. One of the most-parsimonious trees obtained by heuristic searches of the partial ribosomal RNA operon (including partial small subunit, internal transcribed spacer (ITS1) region, 5.8S gene, ITS2, and partial large subunit). Bootstrap values are above the lines at branching points. Asterisks (*) indicate isolates associated with the type material

	DISCUSSION

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Ophiostoma stenoceras clade – The O. stenoceras clade includes 29 isolates, including the strain representing the type of the species (CMW3202) from Norway. Other O. stenoceras isolates from Europe (Italy, Netherlands and France), U.S.A. and New Zealand, as well as isolates resembling O. stenoceras from Africa, South America and Indonesia, grouped together in this clade. This study thus represents the first report of O. stenoceras from Colombia, Kenya, Uruguay, Indonesia and South Africa. In South Africa the fungus is distributed widely on a variety of hardwood hosts.

The fact that three of the O. stenoceras isolates in the study came from humans is of particular significance. The isolate of Mariat (C1189) from healthy human scalp, and which was suggested to represent the teleomorph of S. schenckii (Mariat 1971a), grouped clearly within the O. stenoceras clade. Our data, therefore, confirm previous studies showing that this isolate cannot be considered the teleomorph of S. schenckii (Mendonça-Hagler et al 1974, Suzuki et al 1988).

The O. albidum isolate (C1190) grouped within the O. stenoceras clade. This species originally was described from bark beetle galleries in Sweden and was distinguished from O. stenoceras by its smaller perithecia (Mathiesen-Kåårik 1953). Although other slight morphological differences between the two species have been reported (Kåårik 1960, Mathiesen-Kåårik 1960, Aoshima 1965, Griffin 1968), De Hoog (1974) and Upadhyay (1981) treated O. albidum as a synonym of O. stenoceras. Our results support this synonymy.

The isolate of O. ponderosae (C87) also grouped in the O. stenoceras-clade, and the sequence was identical to that of the strain representing the type of O. stenoceras. In the original description of O. ponderosae, Hinds and Davidson (1975) reported ascospores of 4.5 to 5.5 µm long, while Robak (1932) reported ascospore lengths of 2.0–2.9 µm in the original description of O. stenoceras. In subsequent descriptions of O. stenoceras, however, the range of ascospore lengths was expanded to include lengths of up to 5.5 µm (Davidson 1942, Aoshima 1965, Upadhyay 1981). Ceratocystis ponderosae (= O. ponderosae) was treated by Upadhyay (1981) as a synonym of O. populinum (Hinds & Davidson) de Hoog & Scheffer. Hausner et al (1993), however, suggested that this synonymy might not be valid, based on partial LSU rDNA sequence data. They reinstated the species and transferred it to the genus Ophiostoma (Hausner et al 1993). Our results suggest that O. ponderosae is a synonym of O. stenoceras.

The isolate of O. narcissi (C1468) also grouped in the O. stenoceras clade but differed by 4 bp from other isolates in the group. Limber (1950) mentioned differences in perithecial size and ascospore shape between the two species, and Hunt (1956), De Hoog (1974), Olchowecki and Reid (1973) and Upadhyay (1981) also treated them as separate species. Ophiostoma narcissi originally was isolated from Narcissus bulbs in the Netherlands and has been found on Narcissus bulbs in the United Kingdom (isolate used in this study), New Zealand (Laundon 1973), Canada (Olchowecki and Reid 1973) and the U.S.A. (Upadhyay 1981). Ophiostoma stenoceras typically is isolated from woody substrates and, as was shown in this study, from soil. Although the base-pair differences between O. narcissi and the O. stenoceras isolates might not seem sufficient to distinguish between the species phylogenetically, we believe that the morphological and ecological differences indicate that the two species are distinct. We, therefore, suggest that O. narcissi should be considered distinct from O. stenoceras, until further molecular data of more isolates become available.

The Ophiostoma nigrocarpum clade – This clade contained 14 isolates, which were divided into two smaller clades, each with significant bootstrap support. The larger of the two clades included eight authenticated isolates of O. nigrocarpum from pines and bark beetles in the U.S.A. and Canada. Two Sporothrix isolates from New Zealand (C946 and C1142) also grouped within the main O. nigrocarpum clade, as did the strain associated with the type of O. abietinum (C696). Ophiostoma abietinum originally was described from Abies in Mexico (Marmolejo and Butin 1990) and can be considered an intermediate between O. stenoceras and O. nigrocarpum, based on perithecium morphology (Robak 1932, Davidson 1966, Marmolejo and Butin 1990). The remaining isolate (CMW7131) in the larger O. nigrocarpum clade originated from Quercus in Austria.

The second, smaller clade within the O. nigrocarpum group consists of a South African isolate from Eucalyptus (CMW2543) and a Japanese isolate from Quercus (C818). Since both clades in the O. nigrocarpum group exhibit some variability, we consider this group a poorly understood species complex. Ophiostoma abietinum, therefore, still should be treated as a distinct species until further studies have been conducted.

Sporothrix schenckii clades – Within the larger S. schenckii clade, there are two strongly supported groups of isolates. All isolates from the first group originated from diseased human tissue. This includes the American isolate from a human (ATCC14284), which groups with the South African isolates from humans. With one exception (CMW7613), all the isolates from the second group originated either from soil or plant material. This confirms previous observations in which morphological and physiological differences were observed among isolates of S. schenckii from human tissue and those from other sources (Travassos and Lloyd 1980). Isolates from wood and soil also tend to be less pathogenic to mice (Travassos and Lloyd 1980), suggesting some differences between them. Whether these two groups of isolates represent distinct species needs further evaluation, as does the origin of the human pathogen.

In this study the phylogenetic relationships between O. stenoceras and S. schenckii were resolved. The study also highlighted the need for additional investigations of the O. nigrocarpum complex. Additional isolates and other regions of the genome should be included in such studies. The two clades that are resolved in the S. schenckii group are intriguing and need further investigation, both with more sequences and clinical trials.

	ACKNOWLEDGMENTS

 
We thank the Foundation of Research Development (FRD) and the members of the Tree Pathology Programme (TPCP), South Africa, for financial support. We are grateful to various colleagues listed in Table I for supplying cultures. Doug McNew and Joe Steimel of Iowa State University also made valuable contributions to this study in the identification of cultures and in DNA sequencing.

	FOOTNOTES

 
¹ Corresponding author. E-mail: wilhelm.debeer{at}fabi.up.ac.za

Accepted for publication September 9, 2002.

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Aoshima K., 1965 Studies on wood-staining fungi of Japan [PhD Dissertation]. Tokyo Univ (English summary). 2 p.

Berbee ML, Taylor JW., 1992 18S Ribosomal RNA gene sequence characters place the human pathogen Sporothrix schenckii in the genus Ophiostoma. Exp Mycol 16:87-91

Davidson RW., 1942 Some additional species of Ceratostomella in the United States. Mycologia 34:650-662

———. 1966 New species of Ceratocystis from conifers. Mycopath Mycol Appl 28:273-286

De Hoog GS., 1974 The genera Blastobotrys, Sporothrix, Calcarisporium and Calcarisporiella gen. nov. Stud Mycol 7:1-84

DeScenzo RA, Harrington TC., 1994 Use of (CAT)₅ as a DNA fingerprinting probe for fungi. Phytopathology 84:534-540

Farrell RL, Duncan SM, Ram AP, Kay SJ, Hadar E, Hadar Y, Blanchette RA, Harrington TC, McNew D., 1997 Causes of sapstain in New Zealand. In: Kreber B, ed. Strategies for improving protection of logs and lumber, Proceedings of Symposium, Rotorua, New Zealand, 21–22 November. FRI Bull 204:25-29

Gardes M, Bruns TD., 1993 ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113-118[Medline]

Griffin HD., 1968 The genus Ceratocystis in Ontario. Can J Bot 46:689-718

Harrington TC, McNew D, Steimel J, Hofstra D, Farrell R., 2001 Phylogeny and taxonomy of the Ophiostoma piceae complex and the Dutch elm disease fungi. Mycologia 93:111-136

Hausner G, Reid J, Klassen GR., 1993 On the phylogeny of Ophiostoma, Ceratocystis s.s., and Microascus, and relationships within Ophiostoma based on partial ribosomal DNA sequences. Can J Bot 71:1249-1265

Hinds TE, Davidson RW., 1975 Two new species of Ceratocytis. Mycologia 67:715-721

Hsiau PT-W, Harrington TC., 1997 Ceratocystiopsis brevicomi sp. nov., a mycangial fungus from Dendroctonus brevicomis (Coleoptera: Scolytidae). Mycologia 89:661-669

Hunt J., 1956 Taxonomy of the genus Ceratocystis. Lloyd 19:1-58

Kåårik A., 1960 Growth and sporulation of Ophiostoma and some other blueing fungi on synthetic media. Symb Bot Upsal 16:1-168

———. 1980 Fungi causing sapstain in wood. Swedish Univ Agric Sci, Dep Forest Products, Report Nr R114 1-112

Laundon GF., 1973 Records and taxonomic notes on plant disease fungi in New Zealand. T Brit Mycol Soc 60:317-337

Limber DP., 1950 Ophiostoma on Narcissus bulbs. Phytopathology 40:493-496

Mariat F., 1971a Adaptation de Ceratocystis a la vie parasitaire chez l'animal—Etude de l'aquisition d'un pouvoir pathogene comparable a celui de Sporothrix schenckii. Sabouraud 9:191-205

———. 1971b Adaptation de Ceratocystis stenoceras (Robak) C. Moreau à la vie parasitaire chez l'animal Etude de la souche sauvage et des mutants pathogènes. Comparaison avec Sporothrix schenckii Hektoen et Perkins. Rev Mycol 36:3-25

———, Escudié A, Gaxotte P., 1968 Isolement de souches de Ceratocystis sp. à forme conidienne Sporotrichum, se cuirs chevelus humains et de poils de rats. Comparaison avec l'espèce pathogène Sporotrichum schenckii. CR Hebd Acad Sci, Paris 267:974-976

Marmolejo JG, Butin H., 1990 New conifer-inhabiting species of Ophiostoma and Ceratocystiopsis (Ascomycetes, Microascales) from Mexico. Sydowia 42:193-199

Mathiesen-Kåårik A., 1953 Eine Übersicht über die gewöhnlichsten mit Borkenkäfern assoziierten Bläuepilze in Schweden und einige für Schweden neue Bläuepilze. Medd Statens Skogsforskningsins 43:1-74

———. 1960 Studies on the ecology, taxonomy and physiology of Swedish insect-associated blue stain fungi. Oikos 11:1-25

Mendonça-Hagler LC, Travassos LR, Lloyd KO, Phaff HJ., 1974 Deoxyribonucleic acid base composition and hybridization studies on the human pathogen Sporothrix schenckii and Ceratocystis species. Infect Immun 9:934-938[Abstract/Free Full Text]

Nicot J, Mariat F., 1973 Caractères morphologiques et position systématique de Sporothrix schenckii, agent de la sporotrichose humaine. Mycopath Mycol Appl 49:53-65

Olchowecki A, Reid J., 1973 Taxonomy of the genus Ceratocystis in Manitoba. Can J Bot 52:1675-1711

Otani Y., 1988 Seiya Ito's mycological Flora of Japan. Vol. III. Ascomycotina. No. 2. Onygenales, Eurotiales, Ascosphaerales, Microascales, Ophiostomatales, Elaphomycetales, Erysiphales. Tokyo: Yokendo Ltd. 310 p

Robak H., 1932 Investigations regarding fungi on Norwegian ground wood pulp and fungal infection at wood pulp mills. Nyt Mag Naturvid 71:185-330

Schirp A, Farrell RL, Kreber B., 1999 Effect of New Zealand staining fungi on structural wood integrity of radiata pine. In: Kreber B, ed. The 2nd New Zealand Sapstain Symposium. Proceedings of Symposium, Rotorua, New Zealand, 18–19 November, FRI Bull 215:99-104

Summerbell RC, Kane J, Krajden S, Duke EE., 1993 Medically important Sporothrix species and related ophiostomatoid fungi. In: Wingfield MJ, Seifert KA, Webber, JF, eds. Ceratocystis and Ophiostoma: taxonomy, ecology and pathogenicity. St. Paul, Minnesota: American Phytopathological Society. p 185–192

Suzuki K, Kawasaki M, Ishizaki H., 1988 Analysis of restriction profiles of mitochondrial DNA from Sporothrix schenckii and related fungi. Mycopathologia 103:147-151[Medline]

Swofford DL., 1998 PAUP: phylogenetic analysis using parsimony. Version 4. . Sunderland, Massachusetts: Sinauer Associates

Taylor JJ., 1970 A comparison of some Ceratocystis species with Sporothrix schenckii. Mycopath Mycol Appl 42:233-240

Travassos LR, Gorin PAJ, Lloyd KO., 1974 Discrimination between Sporothrix schenckii and Ceratocystis stenoceras rhamnomannans by proton and carbon-13 magnetic resonance spectroscopy. Infect Immun 9:674-680[Abstract/Free Full Text]

———, Lloyd KO., 1980 Sporothrix schenckii and related species of Ceratocystis. Microbiol Rev 44:683-721[Free Full Text]

Upadhyay HP., 1981 A monograph of Ceratocystis and Ceratocystiopsis. Athens,. Georgia: University of Georgia Press. 176 p

Vismer HF, Hull PR., 1997 Prevalence, epidemiology and geographical distribution of Sporothrix schenckii infections in Gauteng, South Africa. Mycopathologia 137:137-143[Medline]

White TJ, Bruns T, Lee S, Taylor J., 1990 Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds. PCR protocols: a guide to methods and applications. San Diego, California: Academic Press Inc. p 315–322

Wingfield MJ, De Beer C, Visser C, Wingfield BD., 1996 A new Ceratocystis species defined using morphological and ribosomal DNA sequence comparisons. Syst Appl Microbiol 19:191-202

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