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Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands
R.P. Baayen
J.P. Meffert
J. de Gruyter
Mycology Section, Plant Protection Service, P.O. Box 9102, 6700 HC Wageningen, The Netherlands
M. Hooftman
Naktuinbouw, Sotaweg 25, P.O. Box 40, 2370 AA Roelofarendsveen, The Netherlands
K. O’Donnell
Microbial Genomics and Bioprocessing Research Unit, National Center for Agricultural Utilization Research, U.S. Department of Agriculture, Agricultural Research Service, 1815 North University Street, Peoria, Illinois 61604-3999
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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A new disease recently was discovered in begonia elatior hybrid (Begonia x hiemalis) nurseries in The Netherlands. Diseased plants showed a combination of basal rot, vein yellowing and wilting and the base of collapsing plants was covered by unusually large masses of Fusarium macroconidia. A species of Fusarium was isolated consistently from the discolored veins of leaves and stems. It differed morphologically from F. begoniae, a known agent of begonia flower, leaf and stem blight. The Fusarium species resembled members of the F. oxysporum species complex in producing short monophialides on the aerial mycelium and abundant chlamydospores. Other phenotypic characters such as polyphialides formed occasionally in at least some strains, relatively long monophialides intermingled with the short monophialides formed on the aerial mycelium, distinct sporodochial conidiomata, and distinct pungent colony odor distinguished it from the F. oxysporum species complex. Phylogenetic analyses of partial sequences of the mitochondrial small subunit of the ribosomal DNA (mtSSU rDNA), nuclear translation elongation factor 1
(EF-1) and ß-tubulin gene exons and introns indicate that the Fusarium species represents a sister group of the F. oxysporum species complex. Begonia x hiemalis cultivars Bazan, Bellona and Netja Dark proved to be highly susceptible to the new species. Inoculated plants developed tracheomycosis within 4 wk, and most died within 8 wk. The new taxon was not pathogenic to Euphorbia pulcherrima, Impatiens walleriana and Saintpaulia ionantha that commonly are grown in nurseries along with B. x hiemalis. Inoculated plants of Cyclamen persicum did not develop the disease but had discolored vessels from which the inoculated fungus was isolated. Given that the newly discovered begonia pathogen is distinct in pathogenicity, morphology and phylogeny from other fusaria, it is described here as a new species, Fusarium foetens.
Key words: ß-tubulin gene, Fusarium begoniae, Gibberella fujikuroi species complex, Hypocreales, mitochondrial small-subunit ribosomal DNA, morphology, phylogeny, translation elongation factor 1
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, treated as Fusarium sacchari (Butler) W. Gams var. elongatum Nirenberg), which does not produce chlamydospores (Nirenberg and O’Donnell 1998). The begonia pathogen superficially resembled members of the Fusarium oxysporum species complex (FOC) in the production of short monophialides on the aerial mycelium, abundant chlamydospores as well as mainly three-septate macroconidia. Large sporodochial masses consisting of macroconidia covered the base of collapsing plants. Initial diagnostic reports described the fungus as F. oxysporum, and the fungus was first believed to represent a new forma specialis of the FOC.
The begonia pathogen differed phenotypically from members of the FOC, and other known Fusarium species, in the occasional formation of polyphialides in at least some of its strains by having relatively long as well as short monophialides, in its cylindrical conidial masses up to 6 mm high formed on sporodochial conidiomata and in the pungent odor of its colonies. Partial DNA sequences of the EF-1 and ß-tubulin gene exons and introns and the mtSSU rDNA were analysed to assess its phylogenetic relationship to the FOC and related fusaria described by Skovgaard et al (2003) and Geiser et al (2001) that produce both chlamydospores and polyphialides. Genetic variation within the isolates was detected with random-amplified polymorphic DNA (RAPD) finger-printing. The novelty of this rapidly lethal tracheomycosis of B. x hiemalis, suggests that the etiologic agent recently was introduced to Europe, and the isolation of a undescribed Fusarium species from the infected plants appears to support this conclusion. This paper describes the morphology, phylogeny and pathogenicity of this new species, Fusarium foetens Schroers et al.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and representatives of the FOC.
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), potato-dextrose agar (Difco PDA) (Becton Dickinson, Sparks, Maryland), and oatmeal agar (OA, Gams et al 1998), using plastic Petri dishes 9 cm diam. Growth rates and colony diameters of cultures incubated in the dark were measured on SNA and PDA. Characters such as size and shape of conidia, phialides, and chlamydospores were measured from strains grown on SNA incubated in the dark 10–14 d. Sporodochial characters were described from OA after 10–14 d. Presence of polyphialides on SNA and development of sporodochia on OA also was examined in 3–4 wk old cultures. Water was used as mounting medium in microscopic slides. Searches for polyphialides were done after staining the fungal structures with cotton blue in lactic acid. Measurements in the description are given as (i) n1–n2; (ii) n1–n3–n2; or (iii) (n1–)n4–n3–n5(–n2), with n1 = minimum value observed; n2 = maximum value observed; n3 = arithmetical means; n4/n5 = first/third quartile. Macroscopic characters, such as surface texture, odor and colony colors, were described from PDA. Color names are from Kornerup and Wanscher (1978).
Molecular methods. –
For sequencing the partial ß-tubulin gene and for the RAPD fingerprints, mycelium was grown and harvested as described elsewhere (Rehner and Samuels 1994, Schroers 2000) and DNA was extracted using the FastDNA® Kit (Bio 101, Carlsbad, California). Polymerase chain reaction (PCR) was performed in a PCR System 9700 (PE Applied Biosystems, Foster City, California) using the primers T1 and T22 (O’Donnell and Cigelnik 1997), the ramp speeds of the PCR System 9600, and this program: an initial denaturation step at 94 C for 60 s, 35 cycles of 94 C for 35 s, 56 C for 50 s, 72 C for 2 min and a final extension at 72 C for 6 min. Sequencing was performed using the primers T1 and T2 (O’Donnell and Cigelnik 1997) and the BigDye terminator cycle sequencing kit (PE Applied Biosystems, 4303153). The sequences were analysed on an ABI Prism 3700 (PE Applied Biosystems, Foster City, California) using the recommended standard conditions. Sequences of both strands were assembled and edited using SeqMan 3.61 (DNAStar Inc., Madison, Wisconsin). DNA sequences from a portion of the EF-1 gene and the mtSSU rRNA were generated and analyzed according to the procedures described in previous studies (O’Donnell and Cigelnik 1997; Baayen et al 2000, 2001). Maximum-parsimony analyses were performed on the aligned DNA sequences of the individual and combined datasets using PAUP* version 4.0b.4a (Swofford 1999), coding phylogenetically informative indels as a fifth character state. Heuristic searches and parsimony bootstrapping were conducted as described in Geiser et al (2001). DNA sequences have been deposited in GenBank (TABLE I) and the phylogenetic analysis in TreeBase (www.treebase.org) as SN1478 (SN1478–4341 for the matrix and SN1478–4342 for the tree).
Fungal DNA was subjected to RAPD fingerprinting using the phage M13 core sequence (Lieckfeldt et al 1997) (hereafter called M13 primer) and the oligonucleotide primers GC70 (Defontaine et al 2002) and FodB (Manulis et al 1994). Amplification of the DNA fragments was performed by PCR on a PCR System 9700 (PE Applied Biosystems) using the ramp speeds of the PCR System 9600. PCR conditions for the M13 primer were (those for the primers GC70 and FodB are given in brackets): an initial denaturation step at 94 C for 2 min, 40 cycles of 94 C for 60 s, 52 C (35 C) for 60 s, 72 C for 2 min and a final extension at 72 C for 6 min. The reaction volume was 50 µL containing 25 pmol primer (for FodB 20 pmol), 200 µmol of each of the dNTPs (Amersham Biosciences, Uppsala, Sweden), 1x PCR buffer containing 3 mM MgCl2, and 1.5 U of Taq polymerase (Super Taq, HT Biotechnology, U.K.). The amplicons together with a molecular weight marker (Smart-Ladder, Eurogentec, Seraing, Belgium) were separated by electrophoresis in 1.2% agarose gels buffered with 1x TAE (Sambrook et al 1989) and visualized after ethidium bromide staining using a UV transilluminator. RAPD finger-prints were evaluated visually and fragments characteristic of F. foetens were sized using BioNumerics software (Applied Maths, Kortrijk, Belgium, version 2.5).
Pathogenicity testing. – Pathogenicity tests were performed on B. x hiemalis cultivars Bellona, Bazan and Netja Dark, as well as on Cyclamen persicum, Euphorbia pulcherrima Willd. ex Klotzsch, Impatiens walleriana Hook.f. and Saintpaulia ionantha. Rooted plantlets, provided by Florema, Aalsmeer, The Netherlands, were planted in commercial potting soil in 1 L plastic pots and placed in a greenhouse at 23 C (16 h)/20 C (16 h) under a 14 h day (illumination) and 10 h night regime.
In the first trial, B. x hiemalis plants were inoculated with strain CBS 110290 by pouring a 25 mL conidial suspension (106 conidia per mL; prepared by suspending conidia from PDA cultures in sterile water) on the soil. Six plants per cultivar were inoculated by pouring inoculum on the soil without damaging the root system, six plants were inoculated after wounding of the roots by pushing a 1.5 cm wide blade three times into the soil through the root system, four plants were inoculated while wounding the stem base with a blade, and four plants were left untreated to serve as negative controls. Symptom development was followed for 71 d and registered using this index: 0: plants without symptoms; 1: plants with very slight yellowing or slightly delayed growth; 2: plants with definite yellowing or dwarfing, sometimes loss of turgor, otherwise healthy-looking; 3: plants obviously diseased, chlorotic, dwarfed, severe loss of turgor; 4: plants heavily diseased, collapsing, the stem base covered with sporodochia but still alive; 5: plants dead.
In the second trial, E. pulcherrima and I. walleriana (30 plants of each species) were inoculated with CBS 110290 by pouring a 25 mL conidial suspension (106 conidia per mL) on the soil. Fifteen plants per species were left intact during inoculation and 15 plants were wounded by pushing a 1.5 cm wide blade three times into the soil through the root system. Symptom development was followed for 12 wk.
In the third trial, C. persicum and S. ionantha (14 plants of each species) were inoculated with CBS 110290 as described above. Roots of seven plants were wounded as described above and seven plants left intact. Three untreated plants served as negative controls. Symptom development was followed for 12 wk. Corms of C. persicum were dissected at the end of the experiment and examined for vascular discoloration. Fungi were isolated from discolored vessels, and the cultures were identified morphologically and by their RAPD fingerprints.
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RESULTS |
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HOLOTYPUS. THE NETHERLANDS. Cultura sicca (SNA), isolata ex CBS 110286 (= NRRL 31852, PD 2001/7244) HERB. CBS.
Colonies reaching 32–36–43 mm diam on SNA and 30–34–37 mm diam on PDA after 4 d, 57–68–79 mm diam on SNA and 51–62.5–68 mm diam on PDA after 7 d; average radial growth rate on SNA 5.5 mm per d and on PDA 4.8 mm per d. Aerial mycelium white, on SNA sparsely developed, faint, sometimes almost absent but abundantly formed near or on filter paper, consisting of single hyphae or ropes of few hyphae; on OA moderately and evenly produced (FIGS. 21, 22), resulting in a felty to cottony appearance; on PDA abundantly produced, forming thick white tufts evenly covering the whole (FIG. 23) or only irregular portions of a colony. Colony reverse on PDA when incubated in the dark unpigmented in most areas or with spots, sectors, or the central half appearing brownish (6D5), reddish brown (8E6), grayish ruby (12E5), or dark green (29F4); on PDA when incubated under near-UV light with brownish orange to brownish hues (5C5–5D5, 6D5, 6E5), or reddish brown (9D4) to grayish red (10D4); on OA pale orange (5A3), grayish red (10D4–10D5–11D4–11D5), reddish to violet brown (10E3–10E4), or violet brown (10F4). Conidiophores formed laterally from hyphae of the aerial mycelium producing microconidia or in sporodochia producing macroconidia. Aerial mycelium bearing solitary monophialides (FIGS. 1–5), occasionally short supporting cells with whorls of up to 3 monophialides (FIG. 3), or more rarely, solitary polyphialides (FIGS. 6–8); phialides either cylindrical and slightly tapering toward the tip (long phialides in FIG. 5) or narrowly flask-shaped (FIGS. 1, 2), with widest point in the middle, (3.5–)9.5–12.5–14(–33.5) µm long, (1.8–)2.1–2.4–2.6(–3.3) µm wide at base, (2.1–)3.0–3.3–3.6(–4.4) µm at widest point, and (1.1–)1.4–1.5–1.6(–1.9) µm near the aperture (n = 82). Microconidia predominantly 0-septate (FIGS. 13–15) to rarely 3-septate (FIG. 16), held in unpigmented heads; 0-septate conidia ovoidal to ellipsoidal, sometimes allantoidal with hilum mostly visible and apex rounded (FIGS. 13–15), (4.5–)5.5–6.5–7.0(–13.5) x (2.1–)2.5–2.8–2.9(–4.3) µm (n = 438); 1–3-septate conidia fusiform to slightly curved, generally without recognizable foot-cell (FIG. 16); 1-septate conidia (12–)13.5–16–17.5(–24) x (2.6–)3.3–3.4–3.7(–4.2) µm (n = 31). Sporodochia formed on agar surface (FIGS. 21, 22), submerged, or on a prosenchymatous stroma, bearing monophialides that arise laterally in dense aggregations (FIG. 9) or terminally in adpressed whorls from verticillately branched supporting cells (FIG. 10). Macroconidia predominantly 3(–5)-septate, slightly curved; the central two cells frequently almost straight, typically widest in the middle; basal cell indistinctly pedicellate (FIGS. 17–20); 3-septate conidia (22.5–)31.5–34–36.5(– 47.5) x (3.4–)4.2–4.4–4.6(–5.3) µm (n = 387); 4- and 5-septate conidia not conspicuously longer than 3-septate conidia; masses of conidia on SNA flat hemispherical, up to 200 µm diam, pale to light orange (5A3–5A4); masses of conidia on OA up to 6 mm diam, hemispherical to dome-shaped or slightly cylindrical (FIGS. 21, 22), remaining intact for more than 4 wk, typically light orange (5A3) (FIGS. 21, 22), rarely also somewhat bluish; masses of conidia on PDA light orange, brownish orange or light brown (5A4, 5C4, 5D4) when incubated under near-UV light or unpigmented, cream-colored, or grayish blue (23C4) when incubated in the dark. Stromata formed on OA, not observed on PDA or SNA, consisting of pseudoparenchymatous or prosenchymatous cells, in older colonies becoming purple red to blackish green and showing a KOH positive color reaction, in early stages covered with conspicuous aerial mycelium that gives the colonies a dotted appearance (FIG. 21), in older colonies frequently supporting sporodochia. Chlamydospores globose to subglobose, rare or abundant, mostly terminal, smooth or warted, 7–13 x 7–11 µm (FIGS. 11, 12). Odor of colonies on SNA indistinct, of colonies on OA and PDA pungent, irritating. Teleomorph unknown.
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Etymology. – Foetens (Latin), stinking, in reference to the strong odor of colonies grown on OA and PDA.
Known distribution. – Nurseries in The Netherlands and Germany.
Habitat. – On B. x hiemalis, causing tracheomycosis.
Commentary. – Formation of sporodochia, which developed best on OA, probably is stimulated by pieces of oat exposed at the agar surface, particularly at points where the agar surface was disturbed during inoculation. Similar sporodochia also were formed occasionally on PDA.
Phylogenetics. –
Heuristic-parsimony analyses of the combined partial EF-1 (676 bp), ß-tubulin (575 bp), and mtSSU rDNA (713 bp) aligned sequences yielded a single most-parsimonious tree based on 230 parsimony-informative characters (PIC) 392 steps in length with a consistency index (CI) of 0.85 and a retention index (RI) of 0.94. The monophyly of a F. foetens-FOC clade was strongly supported (bootstrap =99%, FIG. 25), and these taxa were reciprocally monophyletic. This clade also was supported by bootstrapping of the individual partitions: EF-1 = 87%, ß-tubulin = 64%, and mtSSU rDNA = 77% (FIG. 25). All 18 strains of F. foetens tested shared identical mtSSU rDNA, EF-1 and ß-tubulin haplotypes. The members of the FOC shown in FIG. 25 represent the three main clades in the FOC (O’Donnell et al 1998b, Baayen et al 2000). The sister group of the F. foetens–FOC clade was unresolved.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Nirenberg and O’Donnell 1998) but occasionally form in some strains of F. foetens. Other characters that distinguish F. foetens from members of the FOC include the length of monophialides formed by the aerial mycelium, which can be up to 35 µm in F. foetens but only 14 µm in the FOC (Gerlach and Nirenberg 1982), well-developed sporodochia, which are present in the FOC only in some cases (Domsch et al 1980), and the strong, unpleasant odor of colonies on OA and PDA, which has not been described for a member of the FOC. However, because of their cryptic nature, these characters might be of limited diagnostic value.
Cultures of F. foetens produced a strong and pungent odor on OA and PDA that was recognizable even around closed Petri dishes. In contrast, the odor of F. commune and many taxa of the Gibberella fujikuroi species complex, including F. begoniae, is described as imperceptible (Nirenberg and O’Donnell 1998, Skovgaard et al 2003) or as "sweetish" (Gerlach and Nirenberg 1982). The odors of Fusarium redolens and some formae speciales of F. oxysporum is described as strong and lilac-like, but most strains of F. oxysporum have no perceptible odor (Gerlach and Nirenberg 1982).
Although some of the characters of F. foetens might be subject to degeneration during storage, we included only recently isolated strains in this study and these showed relatively constant character patterns. Therefore, we conclude that freshly isolated strains of F. foetens should be easily identifiable as distinct from F. oxysporum based on morphological characters. Strains of F. foetens also can be identified by sequencing a portion of the EF-1 or ß-tubulin genes and by RAPD analysis, especially with the GC70 and FodB primers.
Distinction of F. foetens from taxa closely related to the FOC and the G. fujikuroi species complex. –
Polyphialides formed by F. foetens suggest a phenotypic similarity with members of the G. fujikuroi species complex and near relatives including F. miscanthi (Gams et al 1999), F. nisikadoi (Nirenberg and Aoki 1997), F. redolens (Gerlach and Nirenberg 1982), F. hostae (Geiser et al 2001) and F. commune, all of which fall outside of both the G. fujikuroi species complex and the FOC (Gams et al 1999, Baayen et al 2001, Geiser et al 2001, Skovgaard et al 2003). Fusarium miscanthi, which abundantly forms polyphialides, and F. nisikadoi, which produces microconidia in chains, also are phenotypically relatively similar to taxa of the G. fujikuroi species complex in that they have strongly beaked and narrowly tapering macroconidia. In contrast, F. foetens forms polyphialides rarely, produces microconidia in heads and has only moderately beaked macroconidia. Fusarium redolens differs from F. foetens in having wider conidia (Baayen and Gams 1988) and in the lack of polyphialides. Polyphialides are formed both in F. foetens and F. hostae, but the latter species also has wider conidia than F. foetens (Geiser et al 2001). Fusarium foetens shares several features with F. commune, such as the production of microconidia in false heads, the presence of short as well as long monophialides and both branched and unbranched conidiophores, and the ability to form polyphialides as well as chlamydospores. However, F. foetens differs from F. commune in the colony odor, the width of 3-septate macroconidia that are mostly wider than 4.2 µm in F. foetens but generally narrower than 4.2 µm in F. commune (Skovgaard et al 2003) and phylogenetic placement.
Phylogenetic affinities. –
This study provides the first strong bootstrap support for a sister group relationship of the FOC to another Fusarium species. In previous studies, a FOC–F. miscanthi-F. nisikadoi relationship was suggested but weakly supported in bootstrap analyses (Gams et al 1999, Baayen et al 2001). Other taxa, including F. commune (Skovgaard et al 2003) and the G. fujikuroi species complex (O’Donnell et al 1998a, O’Donnell et al 2000), also have been linked to the FOC but with only weak bootstrap support. Phenotypic similarities between F. foetens and the FOC also suggest that these taxa are closely related. However, because F. foetens and FOC members are distinguishable morphologically and they appear to be reciprocally monophyletic in phylogenetic analysis, we conclude that they represent distinct taxa. The absence of nucleotide polymorphisms in the three loci sequenced together with the homogeneous RAPD profiles found among the strains of F. foetens suggests that this species may reproduce clonally. On the other hand, the outbreak strain(s) may be a clonal offshoot of an as yet undiscovered sexual taxon.
Pathogenicity. –
Fusarium foetens is highly aggressive on B. x hiemalis (TABLES II, III). Three cultivars of B. x hiemalis developed severe disease symptoms within 4 wk and were killed 6–8 wk after infection. Symptoms of tracheomycosis suggest that F. foetens invades the plants systemically after initially infecting the roots. Damaging the roots at the time of inoculation considerably enhanced development of the disease; damaging the stem base had a less pronounced effect (TABLE III). Undamaged plants also became diseased and most of them eventually died (TABLE II). It currently is unknown whether other Begonia species, such as B. rex Putz., B. semperflorens Hook., B. tuberosa Herb. Wight ex Wall. and the wild parents of the begonia elatior hybrids, also are susceptible to F. foetens. Other pot plant species grown along with begonia elatior hybrids in commercial greenhouses, such as I. walleriana, E. pulcherrima, S. ionantha and C. persicum, did not develop any visible disease symptoms, suggesting that F. foetens may be relatively host specific. The significance of vascular discoloration in inoculated C. persicum corms requires further study. Although F. foetens was isolated from discolored vessels in the corms of C. persicum, the infection may be an artifact induced by inoculating young plants with a concentrated conidial suspension and simultaneously damaging the roots. Under similar conditions, conidia of F. oxysporum have been shown to enter vessels and to be transported considerable distances into the stems of carnations within 24 h (Baayen and de Maat 1987). This may explain the prominent vascular discoloration inside cyclamen corms and the re-isolation of F. foetens from S. ionantha despite the absence of external symptoms observed in the present study.
Several formae speciales of the FOC cause tracheomycoses similar to that caused by F. foetens on B. x hiemalis. To date, no forma specialis of F. oxysporum has been encountered attacking B. x hiemalis (Wollenweber and Reinking 1935; Domsch et al 1980; Armstrong and Armstrong 1981; Plantenziek-tenkundige Dienst, The Netherlands, unpublished data; NAKTuinbouw, The Netherlands, unpublished data). Furthermore, the potential to induce tracheomycosis is not restricted to the FOC. Host-specific, vessel-colonizing forms also are known in other species such as F. redolens (Baayen et al 2001) and F. udum (Gerlach and Nirenberg 1982). Limited invasion of vessels, although not a typical tracheomycosis, has been reported previously for begonia plants infected by F. begoniae (de Gruyter et al 1994), despite the fact that F. begoniae typically causes corky rot symptoms on leaves, stems and flowers (de Gruyter et al 1994). A vessel-inhabiting or an endophytic to endoparasitic mode of life may be one of the biological strategies followed by various Fusarium taxa including the discussed species.
Origin and epidemiology. –
Begonia x hiemalis have been grown in Europe at least 100 years. The new disease on B. x hiemalis first was observed at the end of 2000, suggesting that F. foetens is a recent introduction. Its pathogenicity to B. x hiemalis suggests that F. foetens may be a pathogen of wild Begonia species, which are native to tropical South America (Simpson and Ogorzaly 1995). Because there are no records of the isolation of this pathogen in Europe before 2000, the fungus might have been introduced into Europe accidentally along with breeding material of wild species. It indirectly might have reached B. x hiemalis nurseries in the Southern Hemisphere from where it was introduced into Europe through trade. Latently infected propagative Begonia material appears to pose a serious risk of spreading F. foetens, and may explain why F. foetens has been isolated in The Netherlands and detected by quarantine inspections in England since the end of 2000.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: Hans.Schroers{at}kis.si
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LITERATURE CITED |
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