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Description of Gibberella sacchari and neotypification of its anamorph Fusarium sacchari

     Department of Plant Pathology, Throckmorton Plant Sciences Center, Kansas State University, Manhattan, Kansas 66506-5502

Brett A. Summerell
Suzanne Bullock

     Royal Botanic Gardens and Domain Trust, Mrs. Macquaries Road, Sydney, New South Wales 2000, Australia

Frank J. Doe

     Department of Biology, University of Dallas, Irving, Texas 75061

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS TAXONOMY NEOTY PIFICATION OF FUSARIUM... DISCUSSION LITERATURE CITED

 

We described the teleomorph of Fusarium sacchari as Gibberella sacchari, sp. nov. This species can be separated from other species of Gibberella on the basis of the longer, narrower ascospores found in G. sacchari and by sexual cross fertility. Female-fertile mating type tester strains were developed that can be used for making sexual crosses with this heterothallic fungus under laboratory conditions. The anamorph, Fusarium sacchari, was neotypified.

Key words: biological species, Fusarium neoceras, Fusarium subglutinans sensu lato, Gibberella fujikuroi mating population B, maize, sorghum, sugarcane

	INTRODUCTION

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Nine mating populations or biological species, denoted by the letters A–I, have been identified within the Gibberella fujikuroi species complex (Britz et al 2002, Samuels et al 2001, Zeller et al 2003). The anamorphs of all nine have unique Latin binomials as do eight of the nine teleomorphs. Our objective in this report is to provide a name and formal description for the teleomorph of the ninth biological species and to describe the mating-type tester strains that are commonly used for identification purposes. To clarify the nomenclature and taxonomy of this taxon we neotypify the anamorph, Fusarium sacchari.

	MATERIALS AND METHODS

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Cultures and culturing conditions.— – Cultures examined were recovered from sugarcane and sorghum and either provided to us or collected by us as indicated in the list below. Strain numbers from other collections are given where known, and are: ATCC—American Type Culture Collection, Manassas, Virginia; BBA—Biologische Bundesanstalt für Land- und Forstwirtschaft, Berlin, Germany; FGSC—Fungal Genetics Stock Center, University of Missouri-Kansas City, Kansas City, Missouri; FRC—Pennsylvania State University, University Park, Pennsylvania; SNS—University of California, Davis, California; KSU—Kansas State University, Manhattan, Kansas; PTS—University of California, Berkeley, California. FGSC and KSU numbers are used preferentially.

When isolates were recovered from plant material, they were plated onto semiselective peptone-PCNB media (Nash and Snyder 1962). After 4–7 d incubation at 25 C, we selected Fusarium colonies that emerged from this material. We purified all cultures, including those received from other investigators, by subculturing single conidia separated by micromanipulation. Isolates were cultured routinely on carnation leaf agar (CLA) (Fisher et al 1982), or on modified Czapek’s complete medium (Correll et al 1987).

All strains are maintained as spore suspensions in 15% glycerol at –70 C. We have deposited a dried culture of FGSC 7610 x FGSC 7611, representing G. sacchari with the National Fungus Collection, Beltsville, Maryland, as BPI 843974. Female-fertile mating-type tester strains (strain numbers KSU B-03853 [= FGSC 7611] and KSU B-03852 [= FGSC 7610]) were deposited as isotypes with the Fungal Genetics Stock Center.

We used this standard Gibberella fujikuroi mating population mating-type tester strains in all mating tests (G. fujikuroi mating population, Gibberella teleomorph, FGSC strain numbers and mating types): G. fujikuroi mating population A, Gibberella moniliformis, FGSC 7600 (MATA-1), FGSC 7603 (MATA-2); G. fujikuroi mating population B, Gibberella sacchari, FGSC 7611 (MATB-1), FGSC 7610 (MATB-2); G. fujikuroi mating population C, Gibberella fujikuroi, FGSC 8931 (MATC-1), FGSC 8932 (MATC-2); G. fujikuroi mating population D, Gibberella intermedia, FGSC 7615 (MATD-1), FGSC 7614 (MATD-2); G. fujikuroi mating population E, Gibberella subglutinans, FGSC 7616 (MATE-1), FGSC 7617 (MATE-2); G. fujikuroi mating population F, Gibberella thapsina, FGSC 7057 (MATF-1), FGSC 7056 (MATF-2); G. fujikuroi mating population G, Gibberella nygamai, FGSC 8934 (MATG-1), FGSC 8933 (MATG-2); G. fujikuroi mating population H, Gibberella circinata, FGSC 9022 (MATH-1), FGSC 9023 (MATH-2); G. fujikuroi mating population I, Gibberella konza, FGSC 8910 (MATI-1), and FGSC 8911 (MATI-2).

Microscopy.— – The description of Gibberella sacchari is based on crosses (FGSC 7610 x FGSC 7611) produced on carrot agar. Perithecia were treated with 3% KOH and 100% lactic acid to observe any color reaction, and measured in situ. Asci and ascospores were mounted in water for measurement and photography. Measurements were taken of 20 each of perithecia, asci and ascospores. Whole perithecia were fixed in 6.5% glutaraldehyde in 100 mM sodium cacodylate buffer at pH 7.6 for 4 h at room temperature (Bullock et al 1980), dehydrated in a graded ethanol series and infiltrated and embedded in LR White resin. Sections 1.5 µm thick were cut with a Reichert ultramicrotome, dried onto poly-L-lysine-coated glass slides and stained with 0.5% toluidine blue O for 10 s (Feder and O’Brien 1968). Sections were mounted in immersion oil. Morphological features of the anamorph (F. sacchari) were photographed in situ on carnation leaf agar. Macro- and microconidia were mounted in water on glass slides and photographed with DIC optics.

Mating-type specific PCR and crossing procedures.— – We identified mating-type idiomorphs (MAT-1 or MAT-2) for the F. sacchari isolates with PCR-based assays, as described in either Kerényi et al (1999) or Steenkamp et al (2000), and in crosses to the female-fertile tester isolates (FGSC 7610 MAT-2 or FGSC 7611 MAT-1) developed as a part of this study. We made crosses on carrot agar as described in Klittich and Leslie (1988).

	RESULTS

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The initial mating-type testers used for this species were the field isolates FGSC 7608 and FGSC 7609. These strains are both highly fertile but are subject to strain degeneration, in which a tough, dense, mycelium with fingerlike projections is produced, with a thinner, wispier mycelium between the denser mycelial fingers. If these colonies are subcultured, then the amount of dense mycelia continues to increase at the expense of the thinner mycelium. The thinner mycelium eventually disappears and only the denser mycelium can be found. Spores from such colonies have an apparently normal ability to serve as a male parent in a sexual cross. When used as a female parent, however, the only portion of the colony on which perithecia form is that with the thinner mycelium. Once the strain produces only the denser mycelium, the colony no longer is useable as a female parent. The frequency with which the dense sectors appear is irregular, but once the process has begun we have not been able to recover a colony that has only the thin phenotype. Instead we begin a new culture from the frozen stock and discard the degenerating culture.

We crossed FGSC 7608 and FGSC 7609 and collected 78 random ascospore progeny. We used these progeny as the female parents in crosses with the parental strains and identified strains that repeatedly produced, at least qualitatively, a large number of mature perithecia. Mating type in all of the progeny was identified on the basis of these crosses. We also identified progeny that retained exclusively the thin phenotype and did not produce sectors with the dense mycelial phenotype in at least three successive subcultures. We selected two progeny (FGSC 7610 and FGSC 7611) based on these criteria and have been using them as the standard testers for this mating population since 1990. We have never seen these testers develop the dense, female-sterile mycelial sectors that can occur in their parents and have not noticed any appreciable reduction in female fertility of these strains over this time.

Members of the B mating population are distinct from other mating populations in the G. fujikuroi species complex in that they do not cross with the testers from any of the other eight described mating populations. Strains listed are cross-fertile with either FGSC 7610 or FGSC 7611 but not with testers for the other known biological species in the G. fujikuroi species complex. In most cases no perithecia are made in the crosses between strains from the different mating populations. On rare occasions a few perithecia may be produced, presumably due to homothallism such as that observed with these testers and a few other strains of mating population B (Britz et al 1999). Thus any crosses in which only a few perithecia are produced on a plate must be viewed as suspect until the progeny produced are shown to have a bi-parental origin.

	TAXONOMY

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Gibberella sacchari Summerell et Leslie sp. nov. FIGS. 1–7

View larger version (114K): [in this window] [in a new window]   FIGS. 1–7. Gibberella sacchari, characteristics of perithecia, asci and ascospores produced from a cross of strains FGSC 7610 x FGSC 7611 on carrot agar. 1–2. Perithecia. 3. Transverse section of a perithecium stained with toluidine blue O. 4. Detail of transverse section of perithecial wall. 5–6. Asci. 7. Ascospores. Bars: 1 and 2 = 200 µm; 3 and 5 = 50 µm; 4, 6 and 7 = 25 µm.

HOLOTYPUS. Cultura exsiccata in agaro ex FGSC 7610 x FGSC 7611.

Etymology.— – Taken from the anamorph, referring to the original host plant, sugarcane.

Teleomorph.— – Perithecia superficial, solitary to aggregated in groups of a few and seated on a minute stromatic base, obovoidal and warty (FIGS. 1–2); 270–390 (mean = 325) µm, 250–390 (mean = 310) µm diam; blue-black, color not changing in 3% KOH, turning red in 100% lactic acid. Perithecial wall 23–39 (mean = 30.6) µm thick laterally, formed of two obvious regions (FIGS. 3–4). Outer wall region 18–33 (mean = 25.6) µm thick; outer cells ± angular to elliptic in transverse section, 5.3–12 (mean = 8.4) µm length x 3.1–5.9 (mean = 4.3) µm thick, with the largest cells at the exterior and the smallest cells toward the interior of the wall, walls of cells 0.5–1.2 (mean = 0.9) µm thick and pigmented. Inner wall region 4.0–5.9 (mean = 4.9) µm thick; cells ± angular to elliptic, 7.2–16 (mean = 10.6) µm length x 1.1–3.2 (mean = 2.2) µm thick. Inner wall cells fusiform, thin-walled and irregular, walls of inner cells 0.3–0.6 (mean = 0.4) µm thick and pigmented (FIG. 4). Outer and the inner wall regions merging imperceptibly; cells of the outer region more pigmented. Perithecial apex continuous with the outer and inner wall layers; cells at the apex smaller appearing as a reticulum; cells forming the ostiolar opening ± clavate and thick-walled at the cell tips; nonpigmented merging periphyses. Cells of the apex attaining the same length to form an apical disk.

Asci fusiform (FIGS. 5–6), regularly dehiscing during slide preparation and 8-spored. Ascospores exuded in a cirrus (FIGS. 1–2), ellipsoidal to obovoid with both ends rounded, 0–1-septate and slightly constricted at the septum, 7.0–8.0 x 3–4.5 (mean 7.6 x 4.2) µm (FIGS. 5–7). Heterothallic species, reproductively isolated from previously described species of Gibberella.

Isolates examined.— – BRAZIL: culture isolated from sorghum by Shirley Nash Smith and received from J. Puhalla and P.T. Spieth 1984, MAT-2, KSU B-00205 (PTS F-1178, SNS Br19a). CHINA: Taiwan, Hsingying; cultures isolated from sugarcane plants by Shirley Nash Smith in 1981 and received from J. Puhalla and P.T. Spieth 1984, MAT-1, KSU B-00281 (ATCC 201263, FGSC 7609, FRC M3128, SNS HY-7, PTS F-1254); MAT-2, KSU B-00278 (ATCC 201262, FGSC 7608, FRC M3127, SNS HY-4, PTS F-1251). EL SALVADOR: La Libertad; cultures isolated from diseased (stalk rot) sorghum plants by L.E. Claflin 2002; all MAT-1, KSU B-12751, KSU B-12752, KSU B-12753, KSU B-12754, KSU B-12755 & KSU B-12756. GERMANY: from Cattleya and received from H. Nirenberg via P.E. Nelson; MAT-2 KSU B-03828 (FRC 1217, BBA 62260). INDIA: all from sugarcane and received from H. Nirenberg via P.E. Nelson; MAT-1, KSU B-03819 (FRC M941, BBA 63340), KSU B-03820 (FRC M942, BBA 63342); MAT-2, KSU B-03821 (FRC M943, BBA 63448). MEXICO: Guadalajara; cultures isolated from diseased (stalk rot) maize plants by L.E. Claflin 2002; MAT-1, KSU B-12747; MAT-2, KSU B-12748, KSU B-12749 & KSU B-12750. PHILIPPINES: Pioneer Overseas Corporation Research Station, Banbic, Calruyao, Laguna; all cultures isolated by J.F. Leslie 1988; from diseased sorghum leaf, MAT-1, KSU B-01722 (FRC M5476), KSU B-01724 (FRC M5478), KSU B-01725 (FRC M5479), KSU B-01726 (FRC M5480); from diseased sorghum stalk, MAT-2, KSU B-01721 (FRC M5467); from sorghum seed, MAT-1, KSU B-01730 (FRC M5484), KSU B-01732 (FRC M5486), KSU B-01735 (FRC M5489); MAT-2, KSU B-01727 (FRC M5481), KSU B-01728 (FRC M5482). USA: Kansas, Manhattan; cultures recovered from a laboratory cross of FGSC 7608 (KSU B-00278) and FGSC 7609 (KSU B-00281) by J.F. Leslie 1989; MAT-1 KSU B-03853 (ISOTY PE, ATCC 201265, FRC M6866, FGSC 7611); MAT-2 KSU B-03852 (ISOTY PE, ATCC 201264, FRC M6865, FGSC 7610).

	NEOTY PIFICATION OF FUSARIUM SACCHARI

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Fusarium sacchari (E.J. Butler) W. Gams first was described as Cephalosporium sacchari Butler from sugarcane in India in 1913 (Butler and Khan 1913) but did not include a description of macroconidia. Cultures with macroconidia were described by Wollenweber and Reinking (1925) as Fusarium neoceras Wollenweber & Reinking. Gams (1971) synonymized the two names to the present form. Because the original type specimen no longer is available we have chosen isolate KSU B-03852 (ATCC 201264, FGSC 7610, FRC M6865) to neotypify the anamorph. Because this isolate is a single ascospore isolate from two parents isolated from sugarcane, has been shown to be conspecific with isolates KSU B-03819 (FRC M941, BBA 63340), KSU B-03820 (FRC M942, BBA 63342); KSU B-03821 (FRC M943, BBA 63448) from sugarcane in India by sequencing and AFLPs (data not shown) and is one of the two parental strains used to create the teleomorph we have chosen it to neotypify.

Neotype, designated here Fusarium sacchari (E.J. Butler) W. Gams. KSU B-03852 (ATCC 201264, FRC M6865, FGSC 7610). A dried culture of this strain is deposited as DAR 76835 at the Plant Pathology Herbarium, Orange Agricultural Institute, Department of Primary Industries, New South Wales, Australia.

Anamorph features (FIGS. 8–13) are similar to those described by Nirenberg (1976) and Gerlach and Nirenberg (1982). Key features are 3–4-septate macroconidia (FIGS. 8–9) and oval microconidia (FIGS. 10–11) borne in false heads on monophialides and polyphialides (FIGS. 12–13).

View larger version (78K): [in this window] [in a new window]   FIGS. 8–13. Characteristics of Fusarium sacchari. 8–9. Macroconidia. 10–11. Oval to obovoid microconidia. 12–13. Microconidia on monophialides and polyphialides produced in carnation leaf agar cultures. Bars = 25 µm.

	DISCUSSION

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Relative to other Gibberella species, the ascospores of G. sacchari are large. In this study the sizes that we measured were 28–32 x 3.0–4.5 (mean 30.4 x 4.2) µm, which is somewhat shorter and narrower than the values observed by Kuhlman (1982) (16–32 x 4–8 [mean 22.4 x 5.6] µm) wide. Kuhlman (1982) found the mean values for the ascospore sizes to be significantly different from the means for G. moniliformis (17.5 x 4.8 µm), G. fujikuroi (12.5 x 4.7 µm), and G. intermedia (14.6 x 4.8 µm). Our observations are consistent with his conclusions. In addition G. sacchari probably can be distinguished from G. nygamai (13.9 x 5.3 µm), G. subglutinans (19.6 x 5.9 µm), G. thapsina (17.0 x 6.0 µm) and G. circinata (12.7 x 5.2 µm) on the basis of the generally longer and narrower ascospores found in G. sacchari. This trait could be especially useful for distinguishing G. sacchari from other species in Fusarium subglutinans sensu lato, which generally are similar morphologically.

With respect to perithecial diameter, the values we obtained (250–390 µm [mean 310 µm]) are somewhat narrower in the range but similar in the mean (240–420 µm [mean 307 µm]) to those reported by Kuhlman (1982). Perithecial diameter could be used to differentiate perithecia of G. sacchari from those of G. fujikuroi (mean perithecial diameter 231 µm), G. thapsina (250 µm), and G. intermedia (389 µm) but not from those of G. moniliformis (321 µm) or G. nygamai (309 µm) and probably not from those of G. subglutinans (336 µm) or G. circinata (337 µm) (Klassen and Nelson 1996, Klittich et al 1997, Kuhlman 1982). The comparative measurements of these different species must be evaluated with caution however because the perithecia and ascospores they contain were grown on several different substrates (e.g. carrot agar, V-8 juice agar and carnation leaf agar) and differences in nutrition could alter the values observed. The degree of maturity of both the perithecia and the spores that they contain similarly could alter the observed sizes of the asci, ascospores and perithecia. Other described Fusarium species to which F. sacchari shows morphological similarity and is closely related (e.g. F. acutatum, F. bulbicola, F. concentricum, F. denticulatum, F. guttiforme, F. pseudocircinatum, F. pseudonygamai and F. ramigenum [Nirenberg and O’Donnell 1998]), have as yet no reported sexual stage, and the utility of ascospore size or perithecial diameter as distinguishing characters for these species remains unknown.

Representative isolates now assigned to G. sacchari often have been included in studies of variation in physiological traits or molecular characters. Differences that separate G. sacchari from the other members of the G. fujikuroi species complex include sensitivity to hygromycin and benomyl (Yan et al 1993), polymorphism in isozyme banding patterns (Huss et al 1996), chromosome length (Xu et al 1995), AFLP banding pattern (Marasas et al 2001) and DNA sequences of representative genes (O’Donnell et al 1998). The only unique isozyme band for G. saccahara is a pattern observed for esterase (Huss et al 1996). However the ß pattern for glucose-4-phosphate isomerase is found only in G. moniliformis and G. sacchari and these two species can be distinguished easily on the basis of the ß pattern for triose phosphate isomerase, which is unique to G. moniliformis. O’Donnell et al (1998) concluded that G. sacchari was related most closely to F. fujikuroi, F. proliferatum, F. globosum and F. concentricum based on the sequence of the ß-tubulin, mitochondrial small subunit rDNA, and 28S rDNA genes. Species to which G. sacchari is more similar morphologically (e.g. G. subglutinans and G. circinatum) were not closely related to G. sacchari when these DNA sequences were used to estimate relatedness. Marasas et al (2001) showed that G. sacchari was distinct from F. andiyazi, F. nygamai, F. pseudocircinatum, F. ramigenum, F. thapsinum and F. verticillioides on the basis of AFLP fingerprinting patterns. Strains of G. sacchari are not known to produce fumonisins (Leslie et al 1992).

The strains examined for this study were from Taiwan, the Philippines, Germany (greenhouse), India, Mexico and El Salvador, but other strains have been reported from Brazil, India, Malaysia, South Africa and Thailand (Leslie 1995). In crosses with the tester strains, however, many of the isolates not included in this study were reported to produce relatively few perithecia, and thus their identity as G. sacchari should be regarded as tentative due to the potential problems associated with selfing by the testers. The host range similarly should be considered limited to maize, sugarcane, orchids and sorghum until the isolates reported from banana, peanut and rice have been examined more closely.

Identification of G. sacchari can be accomplished in many ways. The size of the ascospores and the fertility of the strain in crosses with standard tester isolates are the technically simplest means of distinguishing G. sacchari from other sibling species in the former F. subglutinans sensu lato. The species also can be distinguished based on AFLP patterns, isozymes and by differences in the DNA sequence of several commonly studied genes.

Gibberella sacchari has yet to be reported under field conditions, but the anamorph, F. sacchari, has been recovered from a diverse, although small, set of host plants. The fungus often has been associated with Fusarium sett and stem rot of sugarcane (Egan et al 1997); however no comprehensive studies of host range or pathogenicity have been conducted. Given the recent increase in our knowledge of the taxonomy of this fungus and its close relatives, such studies would be both interesting and important.

	ACKNOWLEDGMENTS

 
This research was supported in part by the Kansas Agricultural Experiment Station and by the Sorghum and Millet Collaborative Research Support Program (INTSORMIL) AID/DAN-1254-G-00-0021-00 from the U.S. Agency for International Development. We thank Larry E. Claflin, John Puhalla, Philip T. Spieth and the late Paul E. Nelson for providing some of the strains used in this study. JFL thanks the Australian-American Fulbright Commission and The Royal Botanic Gardens and Domain Trust, Sydney, for the award of fellowships to support his sabbatical leave in Australia. Contribution No. 03-20-J from the Kansas Agricultural Experiment Station, Manhattan.

	FOOTNOTES

 
Accepted for publication January 6, 2005.

¹ Corresponding author. Department of Plant Pathology, 4002 Throckmorton Plant Sciences Center, Kansas State University, Manhattan, Kansas 66506-5502; Phone: 785-532-1363; Fax: 785-532-2414; E-mail: jfl{at}plantpath.ksu.edu

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