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Systematic Botany & Mycology Laboratory, USDA Agricultural Research Service, Room 304, B011a, 10300 Baltimore Ave., Beltsville, Maryland 20705
Marianne Elliott
College of Forest Resources, University of Washington, Seattle, Washington 98195
Amy Y. Rossman 1
Systematic Botany & Mycology Laboratory, USDA Agricultural Research Service, Room 304, B011a, 10300 Baltimore Ave., Beltsville, Maryland 20705
Robert L. Edmonds
College of Forest Resources, University of Washington, Seattle, Washington 98195
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSTAXONOMYRESULTSDISCUSSIONLITERATURE CITED |
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Pacific madrone (Arbutus menziesii) is a broadleaf evergreen tree native to western North America that has been in decline for the past 30 years. A fungus has been isolated and was verified as the cause of cankers on dying trees. It was determined to belong in the genus Fusicoccum, an asexual state of Botryosphaeria. This genus in both its sexual and asexual states commonly causes canker diseases of deciduous woody plants. Using morphological and molecular data the fungus causing cankers on Pacific madrone is characterized, described and illustrated as a new species of Fusicoccum, F. arbuti D.F. Farr & M. Elliott sp. nov. No sexual state is known for F. arbuti. Evidence from the literature, cultures and specimens suggests that F. arbuti, often mistakenly identified as Nattrassia mangiferae, has been causing madrone canker since at least 1968. Authentic isolates of Nattrassia mangiferae as the synanamorph Scytalidium dimidiatum were sequenced and determined to be different from Fusicoccum arbuti and to belong in Botryosphaeria/Fusicoccum. In addition to molecular sequence data, the morphology of the pycnidial and arthric conidial states of Nattrassia mangiferae/Scytalidium dimidiatum resembles that of Fusicoccum. Therefore the correct name for Nattrassia mangiferae and its numerous synonyms (Dothiorella mangiferae, Torula dimidata, Scytilidium dimidiatum, Fusicoccum eucalypti, Hendersonula toruloidea, H. cypria, Exosporina fawcetii, H. agathidia, and S. lignicola) is Fusicoccum dimidiatum (Penz.) D.F. Farr, comb. nov.
Key words: Arbutus, Botryosphaeria, British Columbia, California, Canada, ß-tubulin, forest pathology, Fusicoccum, Hendersonula, ITS, Nattrassia, Oregon, Scytalidium, systematics, Washington
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSTAXONOMYRESULTSDISCUSSIONLITERATURE CITED |
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, Elliott and Edmonds 2003). Although a number of fungi have been isolated from diseased madrone trees, one species has been consistently associated with cankers (Elliott et al 2002, Elliott and Edmonds 2003). This fungus initially was identified as Nattrassia mangiferae (Syd. & P. Syd.) B. Sutton & Dyko. The objectives of this research were to identify and characterize the fungus causing cankers on Pacific madrone and compare it with N. mangiferae. Molecular data confirm that the fungus causing madrone canker is not N. mangiferae. Rather it is a new species of Fusicoccum Corda, distinct from known species of Fusicoccum, all of which are the asexual states of Botryosphaeria Ces. & de Not. The fungus causing madrone canker is described and illustrated as a new species of Fusicoccum. In addition the phylogenetic placement and accurate scientific name of Nattrassia mangiferae and its synanamorph Scytalidium dimidiatum were determined.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSTAXONOMYRESULTSDISCUSSIONLITERATURE CITED |
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For microscopic examination material was rehydrated and mounted in 3% KOH. Conidiomata were sectioned at ca. 10 µm thick with a freezing microtome. Sections were mounted in lactic acid with cotton blue. Observations of microscopic features were made with a Zeiss Axioplan 2 microscope with bright field and fluorescence illumination. Calcofluor was used as the fluorescent dye. Photographs and measurements of microscopic features were taken with a Spot 2 digital camera (Diagnostic Instruments Inc., Sterling Heights, Michigan) and ImagePro software (Media Cybernetics, Silver Spring, Maryland). The description of cultural characteristics is based on isolates grown at 25 C in the dark on Difco potato-dextrose agar (PDA) for 8 d. The average growth rates were determined based on colony diameter for five replicates grown on PDA in the dark for 8 d at 15, 20, 25, 30 and 35 C. Colors were determined with Kornerup and Wanscher (1978). Cultures were stimulated to sporulate by growing them on oatmeal agar at 25 C in the dark for 1 wk, and under a 12 h light/12 h dark regime for 2 wk as well as on prune agar (3 prunes, 5 g lactose, 1g yeast extract, 17 g agar, 1 L H2O). Cultures sporulated on sterilized woody twigs of Pacific madrone and alfalfa stems (Medicago sativa L.) on water agar under the same conditions listed above; this technique was used to obtain the holotype specimen and dried culture herbarium specimens.
DNA isolation, sequencing and analyses.— –
Isolates were cultured from madrone or obtained from a culture collection. Isolates were grown 7 d in a basal liquid medium (5 g peptone, 0.25 g MgSO4, 0.5 g KH2PO4, 1 L H2O) to prevent melanin formation, which interferes with DNA extraction. Mycelium was dehydrated in acetone (Punekar et al 2003) then ground in microcentrifuge tubes containing the extraction buffer (100 mM Tris-HCl, pH 8.0; 1.4 M NaCl; 20 mM EDTA; 2% CTAB, w/v; 2% mercaptoethanol; 2% PVP) and a small amount of sterile sand. The mixture was incubated 1 h at 65 C. The lysate was extracted with chloroform-isoamyl alcohol (24:1), centrifuged 10 min at 12 000 rpm, then an equal volume of ice-cold isopropanol was added to the aqueous layer. DNA was precipitated overnight at 25 C (Michiels et al 2003). The precipitate was rinsed with 70% ethanol, dried and resuspended in 100 µL sterile deionized water. A total of 10 µg RNAase A was added and the extracts were incubated at 37 C for 30 min. DNA was diluted to a concentration of 1–2 ng/µL in sterile deionized water.
Six isolates of the madrone fungus and three isolates of Fusicoccum dimidiatum are listed (TABLE I) were sequenced with the universal fungal primers ITS1F and ITS4 to amplify the internal transcribed spacer region of the nuclear ribosomal RNA encoding genes. Part of the ß-tubulin gene also was sequenced. PCR and sequencing were done as described for ITS with primers Bt2a and Bt2b for ß-tubulin (Slippers et al 2004a). Each reaction was performed in 50 µL volumes containing 2.5 U Taq polymerase (Fermentas Inc., Hanover, Maryland), 1 x buffer supplied with the enzyme, 3 mM MgCl2, 0.2 mM of each dNTP, 0.2 µM of each primer, and made up to 50 µL with sterile deionized water. Each reaction mixture was overlaid with mineral oil and PCR was carried out in a MJ PTC-100 thermal cycler (MJ Research Inc., Watertown, Massachusetts) according to the this program: denaturation at 95 C for 85 s, followed by denaturation (95 C for 35 s), annealing (55 C for 55 s) and elongation (72 C for 1 min) with increased elongation times of 1 min every 10 cycles, for a total of 32 cycles. DNA was purified with the QIAGEN QIAquick PCR Purification kit (QIAGEN Inc., Chatsworth, California), labeled with ABI Prism BigDye Terminator Cycle Sequencing Kit (PE Biosystems, Foster City, California) and sequenced in the University of Washington Biochemistry DNA Sequencing Facility on an ABI 3700 high-throughput capillary DNA analyzer.
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) along with numbers for sequences obtained from GenBank. DNA sequences (partial 18S, ITS-1, 5.8S, ITS-2, partial 28S) were aligned with Clustal X Multiple Sequence Alignment Program (version 1.81, Mar 2000) with gap opening penalty = 15.00 and gap extension penalty = 6.66. Sequences were truncated at the 5' and 3' ends and manually aligned when necessary with BioEdit v. 5.0.9 (Hall 1999). Phylogenetic analysis was carried out with PAUP* version 4.0b10 (Swofford 2003). Alignment gaps were treated as a fifth character, and all characters were unordered and of equal weight. The heuristic search for maximum parsimonious trees was done using only informative characters in random (stepwise) addition 100 times per replicate. The branch swapping algorithm was tree bisection and reconstruction (TBR). Maxtrees were unlimited and branches of zero length were collapsed. The ITS tree was rooted to the outgroup containing two species of Cercospora (Genbank AY343371
[GenBank]
and AY342272
[GenBank]
) (van Niekerk et al 2004). Most parsimonious trees were saved and branch supports using 1000 bootstrap replicates were calculated. Goodness of fit for these trees was calculated as well as estimated level of homoplasy (consistency, retention and homoplasy indices). A 50% majority rule consensus tree was calculated in PAUP*. Trees were observed with TreeView (Page 1996). To determine the placement of F. arbuti within Botryosphaeria-Fusicoccum, ITS and ß-tubulin sequences from B. australis, B. dothidea, B eucalyptorum, B. luteum, B. parva and B. ribis were subjected to the same analysis as described above for the full ITS dataset. Trees were rooted with the midpoint method. The ITS and ß-tubulin datasets were combined and a partition homogeneity test was performed in PAUP*. All alignments have been submitted to TreeBase as No. SN2105.
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TAXONOMY |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSTAXONOMYRESULTSDISCUSSIONLITERATURE CITED |
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FIGS. 1–10
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Holotypus: UNITED STATES: WASHINGTON, King County, Seattle, Magnolia Bluffs, isolated from cankers of Arbutus menziesii, Oct 2003, collected by Marianne Elliott, isolated by Amy Rossman AR 4036= CBS 116131. The culture sporulated on sterile wood of A. menziesii on water agar, which was dried and deposited as BPI 843970 herein designated HOLOTY PE.
Mycelium immersed, of branched, septate, smooth, hyaline hyphae, becoming brown, constricted with age, forming sparse, brown, thick-walled, intercalary, serial chlamydospores. Conidiomata black, scattered, uniloculate to multiloculate, 0.5–1.5 x 1.5–3 mm, becoming clumped and irregular in shape, papillate. Stromata in longitudinal section of dark brown textura intricata, locule walls of several layers of thick-walled, dark-brown textura angularis, becoming hyaline toward conidiogenous region. Conidiophores reduced to conidiogenous cells. Conidiogenous cells 9.0–16.5 x 2.5–3.5 µm, cylindrical to subobpyriform, hyaline, holoblastic, discrete, determinate, occasionally indeterminate, proliferating percurrently resulting in periclinal thickenings or rarely indistinct annellations, lining inner wall of pycnidium. Conidia obovoid, fusiform, base truncate, apex obtuse to subobtuse, hyaline, guttulate. Older conidia may become brownish and 2-septate before germination. Conidia on sterile wood 18.5–27.8 x 5.5–7.8 µm, average 22.8 x 6.4 µm, L/W ratio 3.6 (n = 235); on oatmeal agar 21.4–30.4 x 4.6–7.6 µm, average 25.7 x 6.4 µm, L/W ratio 4.0 (n = 244); on prune agar 16.8–28.7 x 4.7–7.8 µm, average 22.3 x 6.2 µm, L/ W ratio 3.6 (n = 263). Microconidia cylindric to allantoid, flexuous or somewhat dumbbell-shaped, hyaline, smooth, nonseptate 3.4–6.3 x 1–1.6 µm, average 4.3 x 1.2 µm (n = 37).
Colonies on PDA at 25 C in the dark for 8 d, light yellow (3A5) to olive grey (3E4) or olive brown (4F4), darkest around plug, pigmentation extending about two-thirds of colony width, outer area white, reverse same, surface mycelium cottony except around plug where mycelium is appressed, obscurely zonate, margin irregular. Growth: 25 mm at 15 C, 63 mm at 20 C, 70 mm at 25 C, 37 mm at 30 C, no growth at 35 C. Colonies not producing yellow pigment diffusing into agar.
Specimens/cultures examined. – CANADA. BRITISH COLUMBIA: Nanoose Bay, isolated from canker of A. menziesii, 8 Mar 1972, collected by A. Funk (UAMH 6800); Vancouver Island, Northwest Bay, isolated from canker of Arbutus menziesii, 6 Jan 1972, collected by G. Helem (UAMH 6799). UNITED STATES. CALIFORNIA: Del Norte County, Gasquet, isolated from cankers of A. menziesii, 20 Oct 1998 (UW 52 = CBS 116574, dried culture BPI 863594); Nevada County, Nevada City, isolated from cankers of A. menziesii, 20 Oct 1998 (UW 32 = CBS 116573, dried culture BPI 863593); San Luis Obispo County, isolated from cankers of A. menziesii, Feb 1997 (UW13 = CBS 117090, dried culture BPI 863936); Santa Cruz County, Santa Cruz, isolated from cankers of A. menziesii, 20 Oct 1998 (culture ME 1–4 = CBS 116575, dried culture BPI 863595); Sonoma County, isolated from cankers of A. menziesii, Oct 1998 (UW22 = CBS 117089, dried culture BPI 863937). WASHINGTON: Jefferson County, Port Townsend, isolated from cankers of A. menziesii, 18 Jun 2003, collected by Marianne Elliott, isolated by Amy Rossman (culture ME 7324 = CBS 116576, dried culture BPI 863596).
Host and distribution. – Known only from Arbutus menziesii Pursh (Pacific madrone) in the western United States and Canada from British Columbia to California.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSTAXONOMYRESULTSDISCUSSIONLITERATURE CITED |
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, 12). The aligned ITS dataset contained 484 characters of which 151 were parsimony informative and 333 were constant (FIG. 11). Heuristic searches in PAUP* resulted in 266 most parsimonious trees with length of 322 steps (CI = 0.7640, RI = 0.9345, RC = 0.7140 and HI = 0.2360). In this dataset isolates of Fusicoccum arbuti group together with 81% bootstrap support. Isolates of Fusicoccum dimidiatum group together in a separate clade in Botryosphaeria-Fusicoccum with 100% bootstrap value.
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). Adding more genes to the analysis would provide better statistical support for the final tree, as would eliminating third codon positions in coding regions. The combined dataset contained 870 characters with 97 parsimony informative characters and 773 constant characters (FIG. 12). A total of 104 most parsimonious trees of 132 steps were obtained (CI = 0.8258, RI = 0.9555, RC = 0.7890 and HI = 0.1742). In the two gene dataset, isolates of F. arbuti grouped with bootstrap values of 99% in a well supported clade that is sister of the B. ribis/B. parva clade (FIG. 12).
Morphological analysis.— –
In reviewing the two most recent keys to Fusicoccum, namely Slippers et al (2004a) and Phillips (2004 http://www.crem.fct.unl.pt/botryosphaeria_site/key.htm), Fusicoccum arbuti is readily differentiated from its closest relatives by conidial size. The conidia in culture of F. arbuti (FIGS. 7–8) are longer than those of F. ribis Slippers et al and F. parvum Pennycook & Samuels but are not as long as those of F. aesculi Corda. In addition F. arbuti does not produce a diffuse yellow pigment into the culture medium as in F. luteum Pennycook & Samuels. Fusicoccum arbuti is similar morphologically to F. parvum, anamorph of Botryosphaeria parva Pennycook & Samuels (1985). As in F. arbuti, the conidia of F. parvum occasionally become 2-septate with the central cell becoming noticeably olivaceous to brown before germination as illustrated in Slippers et al (2004a, FIG. 15). Although similar in shape and septation, the conidia of F. arbuti generally are larger than those of F. parvum, which vary from (11–)14–18(–23) x 5–7(–10) µm, average 16.0 x 5.9 µm (Pennycook and Samuels 1985, Slippers et al 2004a). Small microconidia termed spermatia by Pennycook and Samuels (1985) as described for F. parvum were observed in older cultures of F. arbuti (FIG. 9). These also are produced in cultures of F. ribis (Morgan-Jones and White 1987 as Fusicoccum anamorph of B. ribis Grossenb. & Duggar).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSTAXONOMYRESULTSDISCUSSIONLITERATURE CITED |
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). Fusicoccum arbuti can be isolated from the expanding cankers on madrone. If inoculated with this fungus, pycnidia of F. arbuti are observed on the substratum in nature (Elliott pers comm). Although a sexual state never has been seen in nature or in culture, F. arbuti undoubtedly is derived from within Botryosphaeria. Species of Botryosphaeria, primarily in their asexual states of Fusicoccum or related pycnidial genera, are known commonly to cause twig, stem and basal cankers of woody plants (Swart and Blodgett 1998, Besoain et al 2000, Sanchez et al 2003, van Niekerk et al 2004). They also have been reported to cause twig and stem blights (Ko et al 1999) and commonly are isolated as leaf endophytes ( Johnston 1998).
Madrone canker probably has been present in western North America for at least the past three decades. A canker disease on madrone was reported in Washington in the summers of 1968 and 1969 after an "unseasonably hot and dry" summer of 1967 and "an unusually cold, severe period in Jan 1969" (Davison 1972). The causal fungus was reported as Hendersonula toruloidea Nattrass, a synonym of Fusicoccum dimidiatum (see below), although it is likely that this canker was caused by Fusicoccum arbuti. No voucher specimens or cultures exist to verify the causal agent, however this is probably the first report of madrone canker caused by F. arbuti. Later reports of the madrone canker caused by F. arbuti were listed mistakenly as Nattrassia mangiferae, also a synonym of Fusicoccum dimidiatum (Elliott et al 2002, Elliott and Edmonds 2003). Specimens and cultures document the presence of F. arbuti causing madrone canker since 1972 throughout the range of the host (Hunt and Funk 1992).
Placement of Fusicoccum arbuti.— –
The genus Fusicoccum is one of several anamorphs connected with species of Botryosphaeria. In a paper by Crous and Palm (1999) the concept of Fusicoccum was re-evaluated and the genus was typified based on F. aesculi for which a neotype was designated. Fusicoccum had been defined by Sutton (1980) to include "coelomycetes with fusiform, hyaline, non-septate conidia produced holoblastically in stromatic conidiomata" indicating that this genus best could accommodate the anamorphs of B. dothidea and B. ribis. Although the conidia are produced primarily holoblastically, the concept of Fusicoccum had been expanded by Pennycook and Samuels (1985) to include the older conidiogenous cells of F. aesculi that are enteroblastic and proliferate percurrently. Both authors noted that the conidia of Fusicoccum are initially hyaline but may become olivaceous with age and are primarily aseptate, sometimes becoming septate before germination. Although many species have been described as Fusicoccum, the genus now includes only species that have teleomorphs in Botryosphaeria, if known, and are related genetically to the type species, Fusicoccum aesculi (Slippers et al 2004a). For many species of Fusicoccum including F. arbuti, a Botryosphaeria sexual state has not been seen or reported. The sexual state might be formed only rarely or might have been lost, as is the case for many asexually reproducing fungi (Taylor et al 1999).
In the past 10 years molecular sequence data have been applied to the Botryosphaeria complex resulting in a more accurate circumscription of species within this genus (Phillips et al 2002, 2004, Slippers et al 2004a, b, van Niekerk 2004, Zhou and Stanosz 2001). Major groups within Botryosphaeria recently have been recognized that correlate with anamorph genera including Diplodia, Dothiorella, Fusicoccum and Lasiodiplodia (Phillips et al 2004). Fusicoccum arbuti groups with the type species of Fusicoccum, F. aesculi, the anamorph of Botryosphaeria dothidea, the type species of Botryosphaeria (Slippers et al 2004a). Within Botryosphaeria-Fusicoccum several new species have been recognized, most recently, B. protearum Denman & Crous on Protea (Denman et al 2003), Fusicoccum viticlavatum Niekerk & Crous and F. vitifusiforme Niekerk & Crous on Vitis (van Niekerk et al 2004) and B. australis Slippers & Crous on Acacia and Sequoiadendron in Australia (Slippers et al 2004b), Robinia in Portugal and Vitis in South Africa (van Nierkerk et al 2004).
Fusicoccum arbuti belongs in Botryosphaeria-Fusicoccum and is differentiated readily from all other described species based on morphological and molecular data. In both the ITS tree and the combined ITS-ß-tubulin trees the six isolates of F. arbuti form a unique group with 81% and 99% bootstrap values respectively. Based on molecular data, F. arbuti is most closely related to F. parvum and F. ribis. F. arbuti is distinguished morphologically by the conidia (FIGS. 7–8) that are longer than either F. parvum or F. ribis. Fusicoccum ribis also is similar to F. arbuti in producing chains of brown, thick-walled chlamydospores (FIG. 10) (Morgan-Jones and White 1987, Rayachhetry et al 1996).
Fusicoccum dimidiatum, the correct name for Scytalidium dimidiatum and Nattrassia mangiferae.—Fusicoccum arbuti initially was identified as Nattrassia mangiferae based on the 2-septate conidia with a darkened central cell and presence of chlamydospores (Davison 1972, Elliott et al 2002, Elliott and Edmonds 2003). The monotypic genus Nattrassia B. Sutton & Dyko based on the type species N. mangiferae was considered distinct because of the 2-septate conidia that become brown in the middle cell (Sutton and Dyko 1989). A conspecific synanamorph of N. mangiferae was recognized as S. dimidiatum. Three authentic cultures of N. mangiferae as S. dimidiatum (Penz.) B. Sutton & Dyko were examined and included in the molecular analyses. One of these isolates represents the causal organism of a branch wilt disease on Persian walnut trees (Juglans regia L.) in California (Wilson 1947, 1949). These molecular data reveal that N. mangiferae belongs in Botryosphaeria/Fusicoccum, most closely related to B. mamane (Gardner 1997) (FIG. 11). No sexual state is known for N. mangiferae or S. dimidiatum. The characteristics of the pycnidial state of N. mangiferae resemble those of Fusicoccum aesculi and other species of Fusicoccum. Unlike most species in the genus Fusicoccum, the conidia of N. mangiferae often become 2-septate with a brown central cell. In addition to a Fusicoccum pycnidial state, Nattrassia mangiferae produces a synanamorph that consists of chains of brown, disarticulating, arthric conidia. This synanamorph has been referred to as Scytalidium dimidiatum (= S. lignicola Pesante) based on Torula dimidiata Penz. (Ellis 1971, Sutton and Dyko 1989). The synonymous name Scytalidium lignicola is the type species of the genus Scytalidium. This arthric synanamorph of Nattrassia mangiferae can be regarded as a similar but more extensive development of the brown, thick-walled chlamydospores produced by both F. arbuti and F. ribis.
Based on the molecular sequence data that places Nattrassia mangiferae/Scytalidium dimidiatum in Botryosphaeria/Fusicoccum and the morphological similarities of the pycnidial and arthric conidial states to Fusicoccum, this species is recognized in the genus Fusicoccum as follows:
Fusicoccum dimidiatum (Penz.) D.F. Farr, comb. nov.
Torula dimidiata Penz., Michelia 2:466. 1882. (Basionym)
Scytalidium dimidiatum (Penz.) B. Sutton & Dyko, Mycol Res 93:484. 1989.
= Dothiorella mangiferae Syd. & P. Syd. in Syd. et al, Ann mycol 14:192. 1916.
Nattrassia mangiferae (Syd. & P. Syd.) B. Sutton & Dyko, Mycol Res 93:484. 1989.
= Fusicoccum eucalypti Da Camara, An Inst Super Agron 3:32. 1929.
= Hendersonula toruloidea Nattrass, Trans Brit Mycol Soc 18:97. 1933.
= Hendersonula cypria Nattrass, Cyprus Fungi, Nicosia. p 43. 1937.
= Exosporina fawcettii E.E. Wilson, Hilgardia 17:427. 1947.
= Hendersonula agathidis H.E. Young, Queensland J Agric Sci 5:12. 1948.
= Scytalidium lignicola Pesante, Ann Sper Agron N.S. 11: supplement p. cclxv. 1957.
All these fungal names are synonyms (i.e. they refer to the same species). Because the respective type species of these genera are synonyms of F. dimidiatum, Nattrassia and Scytalidium are synonyms of the genus Fusicoccum.
Fusicoccum dimidiatum has been reported on diverse woody plants (Punithalingam and Waterston 1970, Sutton and Dyko 1989, Farr et al 2004) and occasionally is isolated from human skin and nails (Moore 1988, de Hoog et al 2000). Although reported to be cosmopolitan, the diseases caused by this fungus tend to occur in tropical countries as well as California. Symptoms include gummosis and dieback of stone fruit trees in Egypt (Nattrass 1933), branch wilt and drying of grape vines in India and Iraq (Natour and Ahmed 1969, Wangikar et al 1969), branch wilt, decline and death on citrus in Iraq (Alizadeh et al 2000), leaf spot diseases in India (Chandra 1974), leaf spot and dieback of mango in India and Niger (Pandey et al 1981, Reckhaus and Adamous 1987), and tip rot of bananas in Jamaica and Hawaii (Meredith 1963, 1969). In North America F. dimidiatum has been reported in California to cause branch wilt and canker of walnut (Wilson 1947, 1949), dieback and canker of citrus (Calavan and Wallace 1954), secondary canker infection of almond (English et al 1975) and a canker and dieback of Eucalyptus in Arizona (Matheron and Sigler 1993). The temperature minimum (15 C), optimum (30–35 C) and maximum (38–40 C) for growth of F. dimidiatum (Nattrass 1933, Wilson 1947) ranges about 5 C higher than for F. arbuti, which is 10, 25 and 30–35 C respectively (Davison 1972, Elliott 1999).
A recent report of Hendersonula toruloidea causing a foliar disease of strawberry tree (Arbutus unedo) in Greece (Tsahouridou and Thanassoulopoulos 2000) was not documented with a voucher specimen or culture, thus it cannot be determined if the causal agent was actually Fusicoccum arbuti or F. dimidiatum.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: arossman{at}nt.ars-grin.gov
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LITERATURE CITED |
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