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Previous Article | Next Article 
Applied and Environmental Microbiology, September 1999, p. 4071-4076, Vol. 65, No. 9
Agricultural Biotechnology Center,
Gödöll
Received 8 March 1999/Accepted 15 June 1999
Mating type in the Gibberella fujikuroi species complex
is controlled by a single locus with two alleles and is usually
identified following sexual crosses with standard, female-fertile
tester isolates. The mating type alleles have been arbitrarily
designated "+" and " Gibberella fujikuroi is a
complex of at least eight different mating populations (biological
species) that are reproductively isolated and are denoted by letters
(e.g., G. fujikuroi mating population A). Recently, some of
these mating populations have been given Gibberella species
names that parallel the names of their Fusarium anamorphs,
and additional anamorphs have been identified (4, 19, 22,
34). These species have a worldwide distribution and have been
recovered from hosts as diverse as banana, fig, maize, mango, pine,
rice, sorghum, and sugarcane (26). These species also
produce a variety of secondary metabolites and mycotoxins, such as
fumonisins (28, 29, 41), gibberellic acid (43), moniliformin (28), fusaric acid (3), beauvericin
(30), and fusaproliferin (37), that can
contaminate animal feed and human food.
Mating type in filamentous ascomycetes is usually dimictic, with one
locus and two functional alleles (9), often designated MAT-1 and MAT-2 following the convention proposed
by Yoder et al. (51). The alleles are idiomorphs, which
means that they share no significant sequence similarity but do map to
the same position on homologous chromosomes (5). Mating type
genes have been cloned and sequenced from several filamentous
ascomycetes, including Neurospora crassa (11),
Podospora anserina (7), Cochliobolus
heterostrophus (45), and Magnaporthe grisea
(17). Although there is little MAT sequence
similarity across broad evolutionary distances (44), there
is enough sequence similarity in the HMG-box region of the
MAT-2 allele to permit identification of this region by PCR methods.
Mating type has not been well-characterized at the molecular level in
any of the mating populations (biological species) of the G. fujikuroi species complex. Mating type in these fungi is dimictic
and is usually denoted by a base letter (A through H) that specifies
the mating population and a superscript "+" or " Arie et al. (2) designed degenerate PCR primers that could
be used to amplify the HMG box of the MAT-2 region of
various ascomycetes, including representative species of the genera
Cryphonectria, Gaeuemannomyces,
Mycosphaerella, Nectria, Neurospora,
Pyrenophora, and Setosphaeria and 18 species of
the genus Cochliobolus. Our objectives in this study were
(i) to determine if the primer sets developed by Arie et al.
(2) could be used to amplify the MAT-2 HMG box
from strains in the different mating populations of the G. fujikuroi species complex, (ii) to develop PCR primers that are
specific for the MAT-2 allele in this species complex, and (iii) to replace the arbitrary +/ (A preliminary report of the results has been presented previously
[18].)
Strains.
Except for the progeny in the mapping
population used by Xu and Leslie (48, 49) to construct a
genetic map for G. fujikuroi mating population A, all of the
strains which we used are listed in Table
1.
Strains were routinely cultured on
minimal medium (6), if they had no auxotrophic requirements,
or on complete medium (6), if additional nutritional
supplements were needed. All incubations were performed at 25°C under
a 12 h of light-12 h of darkness diurnal cycle. Strains were
preserved for long-term storage as spore suspensions in a
glycerol-water mixture (15:85) frozen at
0099-2240/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Molecular Standardization of Mating Type
Terminology in the Gibberella fujikuroi Species
Complex
, Hungary,1 and
Department of Plant Pathology, Kansas State University,
Manhattan, Kansas 66506-55022
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
" within each biological species, and the
nomenclature is tied to the standard tester strains. We developed a
pair of PCR primers that can be used to amplify a unique fragment of
one of the mating type alleles (MAT-2) from at least seven
of the biological species in this species complex. Based on the
amplification pattern, we propose a replacement for the existing,
arbitrary +/ terminology that is presently in use. The new
terminology is based on DNA sequence similarities between the mating
type allele fragments from the biological species of the G. fujikuroi species complex and the corresponding fragments from
other filamentous ascomycetes.
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
" that
specifies the mating type. The + and designations were arbitrarily assigned by the researchers who described the mating populations, and the + allele from one mating population may or may not be the same at the molecular level as the + allele from another.
terminology presently in use with
terminology that is consistent with known molecular characteristics and
parallels the terminology used for other filamentous ascomycetes.
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
70°C.
TABLE 1.
Fusarium strains used in this study
Sexual crossing protocol. Crosses were made on carrot agar (20) by using standard tester strains (Table 1) as the female parents. Fertile crosses produced perithecia that exuded a cirrhus of ascospores 2 to 4 weeks after fertilization.
DNA manipulation.
DNA was isolated by a
cetyltrimethylammonium bromide (CTAB) procedure modified from the
procedure of Murray and Thompson (32). Briefly, a frozen
sample (approximately 1.5 to 2 g [wet weight]) was ground to a
fine powder under liquid nitrogen with a mortar and pestle. Then we
added 8 ml of hot (65°C) 2% CTAB buffer (2% CTAB, 100 mM Tris-HCl
[pH 8.0], 20 mM EDTA, 1.4 M NaCl). We incubated the sample at 65°C
for 30 min, extracted the preparation once with an equal volume of
chloroform-isoamyl alcohol (24:1), removed the aqueous layer, and
precipitated the crude nucleic acids with an equal volume of
2-propanol. We dissolved the pellet in 1 ml of TE buffer (10 mM
Tris-HCl, 1 mM EDTA; pH 7.4) and extracted it sequentially with equal
volumes of phenol-chloroform-isoamyl alcohol (25:24:1) and
chloroform-isoamyl alcohol (24:1). The last extract (approximately 600 µl) was treated with 1.5 µl of RNase (2 mg/ml), and the remaining
nucleic acids were precipitated with either 2.5 volumes of 95% ethanol
or 1 volume of 2-propanol. The resulting pellet was washed twice with
70% ethanol, dried briefly, and then resuspended in 50 to 100 µl of TE buffer. We estimated final DNA concentrations by using
HindIII-digested bacteriophage 
DNA and an Applied
Biosystems model IS-1000 digital imaging system (Alpha Inotech Corp.,
San Leandro, Calif.); samples and sample dilutions were electrophoresed
in 1% agarose gels.
-32P]dCTP. Stringent
conditions were used for Southern hybridization; i.e., the membranes
were washed first in 2× SSC-0.1% sodium dodecyl sulfate at 25°C
for 20 min and then two times in 0.1× SSC-0.1% sodium dodecyl
sulfate at 65°C for 20 min (1× SSC is 0.15 M NaCl plus 0.015 M
sodium citrate).
PCR products amplified from G. fujikuroi A-00999 were
extracted from an agarose gel with QIAEX II (Qiagen Inc., Chatsworth, Calif.) by following the manufacturer's instructions. Purified DNA
fragments were blunt-end ligated into the EcoRV site of
plasmid pBluescript KS II+ (Stratagene, La Jolla, Calif.).
Amplification conditions. We used degenerate oligonucleotide primers NcHMG1 and NcHMG2 (2) to amplify the putative HMG-box from the G. fujikuroi standard mating type tester strains. The PCR mixtures (50 µl) contained 1× PCR buffer (Promega, Madison, Wis.), 20 ng of fungal DNA, 2.5 mM MgCl2, each deoxynucleoside triphosphate (Promega) at a concentration of 0.25 mM, each degenerate primer at a concentration of 2 µM, and 1 U of Taq DNA polymerase (Promega). For amplification we used the following program: initial denaturation at 95°C for 3 min, followed by 30 cycles consisting of 1 min at 94°C, 30 s at 55°C, and 1 min at 72°C and a final elongation incubation step consisting of 72°C for 10 min. PCR amplification products were separated by electrophoresis in 1.5% (wt/vol) agarose gels, stained with ethidium bromide, and visualized with UV light.
We designed two Gibberella-specific primers, GfHMG1 (5'-ACCGTAAGGAGCGTCACCATT-3') and GfHMG2 (5'-GGGGTACTGTCGGCGATGTT-3'), based on the sequence of the 262-bp putative HMG-box amplification product obtained from G. fujikuroi A-00999 (EMBL accession no. AJ 131527). These specific primers were used to confirm the results obtained from amplifications performed with the degenerate primers, to identify the mating types of previously untested field isolates, and to confirm mating type assignments made by classical genetic analysis of the progeny of laboratory crosses. When the specific primers replaced the degenerate primers, we altered the amplification protocol by increasing the annealing temperature from 55 to 60°C and by reducing the primer concentration from 2 to 0.1 µM.Sequencing protocol. DNA was sequenced with a Sequenase kit (version 2.0; United States Biochemicals, Cleveland, Ohio). Nucleotide sequences were compared by using the GCG software package (8).
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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We used two degenerate oligonucleotide primers, NcHMG1 and NcHMG2 (2), to amplify the MAT-2 HMG box from the tester pairs of mating populations A through G of the G. fujikuroi species complex (Fig. 1A). All of the strains produced a bright band consisting of unincorporated primers, and the two G. fujikuroi mating population D strains each produced an additional amplification product of approximately 800 bp. As the 800-bp amplification product was found in strains of both mating types, this amplification product is not specifically associated with either mating type idiomorph. Another PCR product, which was approximately 260 bp long, was clearly amplified from one member of each of the tester pairs used for mating populations A, C, E, F, and G but not from their counterparts. A similar amplification product was obtained from the representatives of mating populations B and D, but in each case the band was less intense than the bands obtained for the other five mating populations.
|
We cloned and sequenced the 262-bp fragment amplified from G. fujikuroi A-00999. The nucleotide sequence of this fragment, including the intron, was 58 and 62% similar to the nucleotide sequences of the HMG boxes in Neurospora crassa mt a (39) and Podospora anserina FPR1 (7), respectively. The G. fujikuroi mating population A sequence also contains a putative intron (12) at a conserved site between bp 92 and 138.
We used the nucleotide sequence of the putative MAT-2 HMG
box from strain A-00999 to design two primers to be used to amplify the
homologous fragment from any MAT-2 strain of the G. fujikuroi species complex. Primer GfHMG1 corresponds to bases 29 to 49 at the 5' end of the HMG box, and primer GfHMG2 corresponds to
bases 223 to 252 at the 3' end of the HMG box. When we used this pair of primers to amplify PCR products from genomic DNAs of the seven pairs
of mating type testers, a single 213-bp PCR product was generated from
only one of the mating type tester strains for each mating population
(Fig. 1B). We identified PCR amplification products obtained from
GfHMG1 and GfHMG2 that corresponded to the MAT-2 allele in
strains representing matA+,
matB+, matC
,
matD+, matE+,
matF, and matG. We
probed Southern blots of these PCR amplification preparations with the
262-bp HMG fragment cloned from A-00999 and observed strong
hybridization signals under high-stringency conditions (data not
shown). No hybridization was observed when the PCR product amplified
from N. crassa was probed under the same conditions (data
not shown).
Based on amplification patterns such as those shown in Fig. 1, we
assigned MAT-1 and MAT-2 allele designations to
the known mating types (Table 2).
Independent blind tests of the diagnostic ability of GfHMG1 and GfHMG2
were conducted in both Gödöll, Hungary, and
Manhattan, Kans. We examined 128 progeny (49 matA+ progeny and 79 matA progeny) from the mapping population of
Xu and Leslie (48, 49), the 14 standard testers representing
the seven G. fujikuroi mating populations, and 48 field
strains representing five of the seven mating populations,
Fusarium oxysporum, and Gibberella zeae (Table
1). For these tests, the strains were coded such that we knew the
mating population to which a strain belonged but did not know its
mating type. The results of the PCR amplifications were identical to
the results of the sexual crosses with standard strains. Thus, the PCR
results were predictive of the crossing results, and the crossing
results were predictive of the PCR results. Four of the eight F. oxysporum strains examined had a PCR amplification product
indicative of the MAT-2 allele. No PCR amplification
products were observed with either G. zeae strain.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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We sequenced and analyzed a 262-bp fragment resulting from
PCR amplification of A-00999 DNA by using the NcHMG1 and NcHMG2 primers
(2) and then designed two new primers, GfHMG1 and GfHMG2, based on the sequence obtained. Three lines of evidence suggest that
the 262-bp fragment is part of one of the MAT alleles of G. fujikuroi. First, the fragment shares significant
sequence similarity with N. crassa mt a-1 and P. anserina FPR1. Second, in the 52 field strains belonging to the
seven different mating populations examined, the fragment is
consistently associated with only one mating type within a mating
population. Finally, the presence of the amplified fragment
cosegregated with the matA+ mating type and the
absence of the fragment cosegregated with the
matA mating type for 128 progeny of the
mapping population previously used to construct a G. fujikuroi genetic map (48, 49). On the basis of these
classical genetic mapping data, the amplified fragment maps with 95%
certainty to a 2.3-map unit region that includes MAT and is
unlikely to map more than 1 map unit from MAT if it is not
coincident with it.
Based on the genetic mapping data and the correlations observed with
mating type in the field strains, we propose that the current
nomenclature (e.g., matA+ and
matA) be replaced with new terminology (e.g.,
MATA-1 and MATA-2) (Table 2). The new terminology
includes the mating population with which an allele is associated
because of the multiple biological species in the G. fujikuroi species complex and the potential for significant differences in the sequences associated with different biological species. Such differences might be exploited to design primers that are
specific for both mating population and mating type. If a single
species is identified by name (e.g., Gibberella moniliformis instead of G. fujikuroi mating population A), then the
letter in the gene symbol for the mating population is not needed and may be deleted.
We scored MAT-1 as the absence of the MAT-2 amplification product. The accuracy of scoring could be increased if primers were available to amplify a specific fragment from MAT-1 as well, since at the moment, anything that results in no amplification automatically leads to a diagnosis of MAT-1. Development of a system in which positive results are used to identify both MAT alleles (40) is probably essential for studying the molecular basis of homothallism in G. zeae (33) and G. fujikuroi mating population B (4).
The lack of amplification in the G. zeae strains may have several causes. First, the HMG box-containing MAT allele may be absent, as it is in some homothallic Neurospora species (10, 11). Alternatively, the sequence may be present but divergent enough from the sequences of strains in the G. fujikuroi species complex that amplification does not occur. Finally, it is possible that some G. zeae strains have MAT-1 and some have MAT-2 and that the two strains which we examined had only MAT-1. Based on preliminary reports (52), it appears that some G. zeae strains have coding sequences from both MAT-1 and MAT-2. Presumably, the region corresponding to either GfHMG1 or GfHMG2 was altered in the fusion process, which resulted in no amplification in a PCR when this primer pair was used.
We examined both of the strains (B-03852 and B-03853) that Britz et al. (4) identified as occasionally homothallic. One of these strains (B-03852) clearly yielded a MAT-2 PCR amplification product, while the other strain did not. Thus, the homothallism in these strains cannot be due to mating type switching, as has been observed in some yeasts and filamentous fungi (13-15, 31, 36, 42). Molecular scoring of mating types should reduce the amount of effort required to screen field populations for sexual fertility and should increase the efficiency of the process through which new mating populations are identified by 50 to 75%, since only strains known to differ in mating type need to be crossed.
The availability of molecular diagnostic tools for mating type also may enable workers to analyze purportedly asexual fungi, including Fusarium oxysporum and 12 of the 13 new Fusarium taxa recently described by Nirenberg and O'Donnell (34) and Nirenberg et al. (35). There is circumstantial evidence that sexual reproduction occurs in F. oxysporum, and this evidence is in the form of high levels of diversity with respect to the multilocus vegetative compatibility trait (1, 23, 25, 46), especially in populations of putatively nonpathogenic strains. As Leslie and Klein (27) have shown, sexual reproduction need not be frequent to play an important role in the maintenance and generation of genotypic diversity in field populations of fungi. The availability of mating type data should make it easier to identify potentially cross-fertile strains that can be used to test some of these hypotheses.
In conclusion, our work shows that one of the MAT idiomorphs
of G. fujikuroi contains an HMG fragment that is similar to
a mating type idiomorph found in other model and economically important filamentous ascomycetes. We anticipate that the similarities which have
been observed mean that we will be able to apply much of the
information obtained from studies of other filamentous ascomycetes, such as Neurospora, Podospora, and
Cochliobolus, to members of the G. fujikuroi
species complex without any major changes. By standardizing the
nomenclature from the present A+/A form to
the MAT-1/MAT-2 form, we hope to improve communication between researchers who study filamentous fungi and to establish a
terminology in which all of the mating types are named based on
molecular structure rather than the arbitrary choices of numerous researchers.
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ACKNOWLEDGMENTS |
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This research was supported in part by Hungarian State Research Grant OTKA T 019315, by the Kansas Agricultural Experiment Station, and by the International Sorghum and Millet Collaborative Research Support Program (INTSORMIL) USAID.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Plant Pathology, 4002 Throckmorton Plant Sciences Center, Kansas State University, Manhattan, KS 66506-5502. Phone: (785) 532-1363. Fax: (785) 532-2414. E-mail: jfl{at}plantpath.ksu.edu.
Contribution no. 99-376-J from the Kansas Agricultural Experiment
Station, Manhattan.
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Materials and Methods
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Discussion
References
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