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Department of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0002, South Africa
Anne E. Desjardins
Mycotoxin Research Unit, National Center for Agricultural Utilization of Research, USDA, Agricultural Research Services, 1815 N University Street, Preoria, Illinois 61604
Walter F.O. Marasas
PROMEC, Medical Research Council, P.O. Box 19070, Tygerberg 7505, South Africa
Michael J. Wingfield
Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0002, South Africa
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ABSTRACT |
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Fusarium isolates that form part of the Gibberella fujikuroi species complex have been classified using either a morphological, biological, or phylogenetic species concept. Problems with the taxonomy of Fusarium species in this complex are mostly experienced when the morphological and biological species concepts are applied. The most consistent identifications are obtained with the phylogenetic species concept. Results from recent studies have presented an example of discordance between the biological and phylogenetic species concepts, where a group of F. subglutinans sensu stricto isolates, i.e., isolates belonging to mating population E of the G. fujikuroi complex, could be sub-divided into more than one phylogenetic lineage. The aim of this study was to determine whether this sub-division represented species divergence or intraspecific diversity in F. subglutinans. For this purpose, we included 29 F. subglutinans isolates belonging to the E-mating population that were collected from either maize or teosinte, from a wide geographic range. DNA sequence data for six nuclear regions in each of these isolates were obtained and used in phylogenetic concordance analyses. These analyses revealed the presence of two major groups representing cryptic species in F. subglutinans. These cryptic species were further sub-divided into a number of smaller groups that appear to be reproductively isolated in nature. This suggests not only that the existing F. subglutinans populations are in the process of divergence, but also that each of the resulting lineages are undergoing separation into distinct taxa. These divergences did not appear to be linked to geographic origin, host, or phenotypic characters such as morphology.
Key words: Fusarium subglutinans, maize, reproductive isolation, teosinte
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INTRODUCTION |
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, O'Donnell and Cigelnik 1997, O'Donnell et al 1998a, 2000a, Steenkamp et al 1999, 2000a, 2001). In the global environment, species in this complex are important, because of their association with diseases of agronomically important plants (Correll et al 1991, Leslie 1995, Leslie et al 1990, Sun and Snyder 1981, Varma et al 1974, Ventura et al 1993). These fungi also affect human and animal health, since many species produce toxic secondary metabolites such as moniliformin, beauvericin, fumonisin, fusaproliferin, and fusaric acid (Leslie et al 1992, Logrieco et al 1993, Marasas et al 1983, Sewram et al 1999a, 1999b, Shephard et al 1999, Vesonder et al 1995).
The taxonomy of Fusarium species in the G. fujikuroi complex has been subject to much controversy (Leslie 1995). This is mainly due to a lack of consensus among researchers on how to define a morphological species for the fungi in this complex (Gerlach and Nirenberg 1982, Nirenberg and O'Donnell 1998, Snyder and Hansen 1945). In an attempt to resolve this problem, a biological species concept (Dobzhansky 1937, Mayr 1940) was introduced, whereby eight biological species have been identified (Britz et al 1999, Hsieh et al 1977, Klittich and Leslie 1992, Kuhlman 1982, Leslie 1991, 1995, 1996). These biological species were designated as mating populations A to H, where mating population E, for example, represents F. subglutinans (Wollenw. & Reinking) Nelson, Toussoun & Marasas sensu stricto (Britz et al 1999, Hsieh et al 1977, Klittich and Leslie 1992, Kuhlman 1982, Leslie 1991, 1995, 1996). The eight biological species, however, exclude the more than 80% of species in this complex with no apparent sexual reproductive cycle. Currently, the only method for classifying all the fungal strains in the G. fujikuroi species complex is through the application of the phylogenetic species concept (Cracraft 1983, Taylor et al 2000). With this method, fungi in the G. fujikuroi complex are classified into more than 40 different phylogenetic species (O'Donnell et al 1998a, Steenkamp et al 1999, 2000a).
In a recent study, ten additional phylogenetically distinct species in the G. fujikuroi complex were reported (O'Donnell et al 2000a). Among these was a F. subglutinans strain associated with maize in South Africa, that had previously been classified in mating population E of the G. fujikuroi species complex using the biological species concept (Steenkamp et al 1999). Application of the phylogenetic species concept has, however, indicated that this biological species is subdivided into more than one phylogenetic lineage (O'Donnell et al 2000a, Steenkamp et al 1999, 2001). These lineages may either reflect species divergence within F. subglutinans or are simply the result of intraspecific diversity. However, all of the studies dealing with the molecular classification of strains representing F. subglutinans were based on small sets of different isolates (O'Donnell et al 2000a, Steenkamp et al 1999, 2001) and no definite conclusions could be drawn on the taxonomic status of these fungi. Clarification of the relationships among different F. subglutinans isolates would undoubtedly shed light on how the phylogenetic species concept might influence our interpretation of the biological species concept in the G. fujikuroi species complex. The aim of this study was, therefore, to address the phylogenetic status of members of F. subglutinans by (i) including strains isolated from maize and its wild teosinte relatives from a wide geographic range; (ii) obtaining DNA sequence data from six nuclear regions for these strains; and (iii) using phylogenetic concordance analysis (Avise and Ball 1990, Taylor et al 2000) to determine whether these isolates are interbreeding in nature and, if not, to define sub-groups within F. subglutinans.
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MATERIAL AND METHODS |
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). A portion of three nuclear genes, histone H3 (Glass and Donaldson 1995), calmodulin (Carbone and Kohn 1999) and ß-tubulin (Glass and Donaldson 1995), were amplified from all 31 isolates. We also used an additional set of primers that amplify three unlinked nuclear regions of unknown function (H. Britz unpubl). The first primer set is HB9-a (5'-tcaatacccctcgcctagaa-3') and HB9-b (5'-gaccacagcctcgagaacat-3'), the second is HB14-a (5'-ttccaccatgagaggaaaccc-3') and HB14-b (5'-ccattgccaatcttgatcct-3'), and the third HB26-a (5'-gacttgagtatctgcactgc-3') and HB26-b (5'-gaatgtactactcgacgtcg-3'). For amplification of all these loci, the PCR mixture contained 1 mM deoxynucleotide triphosphates (0.25 mM each), 2.5 mM MgCl2, 0.2 µM of each primer, 0.25 ng/µL DNA, 0.05 U/µL of Super-Therm DNA polymerase [Southern Cross biotechnology (Pty.) Ltd., Cape Town, South Africa] and 1 x Super-Therm reaction buffer. PCR-cycling conditions were as follows: denaturation at 92 C for 20 s, annealing for 20 s at 55 C (calmodulin, tubulin, and histone) or 47 C (HB9, HB14, and HB26), and elongation for 20 s at 72 C. This was repeated 30 times and was preceded by an initial denaturation at 92 C for 1 min and followed by a final elongation step at 72 C for 5 min.
After PCR, the products were purified with a QIAquick PCR Purification Kit (Qiagen GmbH, Hilden, Germany) and sequenced in both directions with the respective primers. Reactions were performed on an ABI PRISMTM 377 automated DNA sequencer, with an ABI PRISMTM Dye Terminator Cycle Sequencing Ready Reaction Kit (Perkin Elmer, Warrington, United Kingdom). Sequences were analyzed with Sequence Navigator version 1.0.1.TM (Perkin Elmer Applied BioSystems, Inc., Foster City, California).
Phylogenetic analyses –
The data sets obtained for each primer set were aligned manually by inserting gaps (TreeBase accession numbers S789 and M1249). Phylogenetic analyses were performed with PAUP (Phylogenetic Analysis Using Parsimony) version 4.0b1 (Swofford 1998), with gaps treated as fifth characters in heuristic parsimony searches, and with tree-bisection-reconnection (TBR) branch swapping and MULTREES (saving of all optimal trees) effective. For bootstrap analyses 1000 replications were performed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Maynard Smith and Smith 1998, Taylor et al 1999b).
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Phylogenetic analysis of the combined data set from all the isolates included in this study revealed the presence of two distinct groups among the isolates associated with maize and teosinte (Figs. 2 and 3). They were designated as Group 1 and 2 (Fig. 3). The genotypes 1-1, 1-2, 1-3 and 1-4 were present in Group 1 and the genotypes 2-1, 2-2 and 2-3 were present in Group 2 (Figs. 2 and 3). Although this clustering pattern was not immediately detectable from the individual gene trees, the combined gene genealogy was not discordant with any of them.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Geiser et al 1998, Koufopanou et al 1997, O'Donnell et al 1998b, 2000a, b, Taylor et al 1999a, b, 2000). Based on previous work (Steenkamp et al 1999, 2001), our null hypothesis was that the set of isolates associated with maize and teosinte, from a wide geographic range, would form part of the existing E-mating population of the G. fujikuroi species complex (i.e., F. subglutinans sensu stricto), and that the observed sequence variation merely reflect intraspecific diversity. However, considering the data generated in this study, we had to reject this hypothesis. The results clearly showed that F. subglutinans is separated into reproductively isolated populations that probably constitute separate sibling species.
The basic rationale behind the use of phylogenetic concordance analyses involves the detection of congruence or the lack thereof, among different gene trees (Avise and Ball 1990, Dykhuizen and Green 1991, Taylor et al 1999a, 1999b, 2000). Incongruence among gene trees from different loci indicates interbreeding among individuals, since sexual recombination ‘reshuffles' their genomes. In an interbreeding population this ‘reshuffling’ results in unique evolutionary histories for the genes in a specific individual, while the genes from different individuals share numerous characteristics or polymorphisms. In reproductively isolated populations genes do not normally flow among individuals, resulting in a lack of shared polymorphisms and consequently perfectly congruent gene trees. Our analyses showed that the evolutionary histories of the six nuclear regions were perfectly congruent in each of the F. subglutinans individuals studied. This is because every gene tree, as well as the one generated from the combined data, was of minimum length (Figs. 1 and 2). The F. subglutinans isolates from the United States, South Africa, Mexico, and Guatemala thus appear to represent reproductively isolated populations.
The tree generated from the combined data separated the 29 F. subglutinans isolates into seven groups (Fig. 2). These groups corresponded to the seven multilocus genotypes identified from the sequence comparisons (Table II). The evolutionary histories for each of the six nuclear regions in all the isolates from genotype 1-1, for example, are identical, indicating a lack of genome ‘reshuffling’ through sexual reproduction. All the isolates in genotype 1-1 can, therefore, be considered as clones of one another, since there is no evidence of interbreeding. The same is also true for genotypes 1-4, 2-1, 2-2 and 2-3. Although genotypes 1-2 and 1-3 are represented by single isolates, analysis of additional isolates will most likely reveal a similar trend. In theory, the overall lack of shared polymorphisms in the six nuclear regions among the seven groups or genotypes, separate the 29 isolates into seven clones, a notion that is probably not entirely correct (see below).
In light of similar studies on other fungi (reviewed by Taylor et al 1999a, 1999b, 2000) our results were rather unexpected. In most of these studies, phylogenetic concordance analysis revealed the presence of so-called cryptic species where individuals from one species were shown to be reproductively isolated from those in the other species. However, these tests also detected that individuals within some of these cryptic species were interbreeding in nature, because of the presence of numerous shared polymorphisms. As a result, generation of consensus trees from combined sequence data resulted in trees that were longer than the expected minimum (observed tree length > number of polymorphic characters). In contrast, the observed tree length in our study was equal to the number of polymorphic characters (Table III), providing no evidence for interbreeding among any of the seven F. subglutinans genotypes. By employing phylogenetic concordance analysis, our study is one of few, and perhaps the first to suggest that a group of fungi capable of interbreeding in the laboratory appears to be propagating exclusively asexually in nature.
The idea that isolates of F. subglutinans exist in clonal populations is not congruent with previous reports. Based on analyses of phenotypic characters, isolates of a specific genotype do not always display similar degrees of resistance to antimicrobial agents and demonstrate similar abilities to produce mycotoxins (Desjardins et al 2000, Marasas et al 1983, 1984, Sewram et al 1999a, 1999b, Shephard et al 1999, Yan et al 1993). For example, the two isolates in genotype 2-2 are significantly different in their resistance to hygromycin B (Yan et al 1993) and the three South African isolates of genotype 1-1 produce markedly different levels of moniliformin and fusaproliferin (Sewram et al 1999a, 1999b, Shephard et al 1999). Another trait suggesting that isolates with similar genotypes are not ‘true clones' is the distribution of mating type. If all the isolates with a specific genotype are clones of one another, their mating types determined using either laboratory crosses or PCR-based methods (Steenkamp et al 2000b) should be the same. Among the F. subglutinans isolates studied, this was not the case, because each of the five multi-isolate genotypes was represented by both MAT-1 and MAT-2 isolates (Desjardins et al 2000, Steenkamp et al 2000a, Yan et al 1993). This variation within groups of isolates with the same genotype, was undoubtedly generated by earlier sexual recombination events. Even though we did not include sufficient isolates and polymorphic loci to address questions on the reproductive mode of F. sublutinans, our results suggest that sexual reproduction is not a common phenomenon. Among the 17 polymorphic sites analyzed, all were fixed within isolates associated with a specific genotype. It is possible that the inclusion of additional data, especially those associated with mycotoxin production, antibiotic resistance and mating, will result in the identification of non-fixed or shared polymorphism. However, the ongoing absence of sex will also bring about fixation in these characters and eventually the absence of shared polymorphisms. Our results, therefore, suggest F. subglutinans populations are diverging into various reproductively isolated lineages that will most probably each eventually constitute separate species.
Classifying the isolates used in this study into their smallest diagnosable units or redefining species limits in the existing F. subglutinans sensu stricto is problematic. Given that sexual reproduction between these isolates appears to be absent in nature, the biological species concept cannot be applied. The phylogenetic species concept assists to some extent, but as shown above, it identifies ‘clones’. Determining whether these ‘clones' represent separate species is an arbitrary exercise, since it is impractical to designate each clonal population as a distinct species. Likewise, to classify each as the same species would be incorrect and would not reflect the natural situation. Separating F. subglutinans into smaller units/taxa is further complicated by the fact that some isolates differ by no more than a single nucleotide at the six nuclear regions analyzed and display no known or diagnosable phenotypic differences. Among the isolates studied, we have, however, observed two major phylogenetic groups (groups 1 and 2) (Fig. 3), which may represent a species partition where groups 1 and 2 represent cryptic species. Genotypes 1-1, 1-2, 1-3 and 1-4 would belong to group 1 and 2-1, 2-2 and 2-3 would belong to group 2. Whether this partition will prove to be diagnosable using phenotypic characters remains to be tested.
There are no apparent links between the genotype to which the F. subglutinans isolates belong and geographic origins or host (Fig. 3). South African isolates were present in all genotypes except 1-2, 1-3 and 2-2, while Mexican/Guatemala isolates were present in all but genotype 2-2. The United States isolates appeared to be restricted to genotypes 2-1, 2-2 and 2-3. Isolates from maize were present in all genotypes except 1-2 and 1-3, while those from teosinte were only absent from genotype 2-2. From the limited data available, the separation of F. subglutinans into the seven genotypes/groups also does not appear to be linked to mycotoxin production (Desjardins et al 2000, Marasas et al 1983, 1984, Sewram et al 1999a, 1999b, Shephard et al 1999) or morphology (Desjardins et al 2000, Steenkamp et al 1999, 2001). There were also no apparent links between the Groups 1 and 2 separation and geographic origin, host or mycotoxin production (Fig. 3) (Desjardins et al 2000, Marasas et al 1983, 1984, Sewram et al 1999a, 1999b, Shephard et al 1999, Steenkamp et al 1999, 2001). Noticeably, maize in the United States is associated only with group 2, but this is probably a sampling effect. The 17 polymorphic sites, therefore, appear to be the only diagnosable features separating the seven genotypes and Groups 1 and 2. As with other fungi (Geiser et al 2000, Peng et al 1999, Taylor et al 2000), our results may lead to the future identification of morphological, physiological, pathogenic, or toxigenic characters supporting either the presence of Groups 1 and 2 or their sub-lineages.
Based on the results presented here, we have attempted to interpret the findings of previous mating studies (Desjardins et al 2000, Steenkamp et al 1999, 2001). Again, there was no relationship between the genotype represented and ability to sexually interact in the laboratory. The genotype 1-1 isolate MRC1084 from South African maize, for example, was capable of producing fertile offspring when mated with genotype 1-3 and 2-1 isolates. Many other isolates were also capable of successful sexual interaction with isolates displaying genotypes other than their own. The presence of the two proposed cryptic species helped to clarify some of the problems that were encountered in previous mating studies (Desjardins et al 2000, Steenkamp et al 1999, 2001). For example, some of the F. subglutinans strains that were collected from maize and teosinte in Mexico and Central America were sexually incompatible with those from the United States (Desjardins et al 2000). As revealed here all the available F. subglutinans isolates from the United States belong to Group 2, whereas those from Mexico and Central America belong to both Groups 1 and 2, which may partially explain their incompatibility. Our results can, however, not explain why the United States isolates were sexually incompatible even with the Mexican strains from Group 2, or why most of the isolates collected from Mexico and Central America are capable of fertile sexual interaction, even though they represent separate cryptic species. Inclusion of all 29 isolates in a mating study might eventually shed light on the connection between the ability to reproduce sexually and genotype/cryptic species, but conditions in the laboratory do not necessarily mimic those in nature. Many fungi are able to sexually interact across the species barrier (e.g., Vilgalys and Sun 1994), which was also demonstrated for strains of F. subglutinans and F. circinatum (Desjardins et al 2000, Steenkamp et al 2001).
The inconsistency between the biological and phylogenetic species concepts illustrated in this study introduces serious complications for the classification of fungi, especially those in the G. fujikuroi species complex, since classification relies heavily on both concepts. Problems with using the morphological species concept have been reported by many workers (O'Donnell et al 1998a, 2000a, Steenkamp et al 1999, 2001), but the current study is the first to report disparities using the biological species concept for classifying fungi in the G. fujikuroi species complex. Undoubtedly, species recognition using phylogenetic concordance analysis will yield the most informative results, but there are two major problems associated with the use of this approach. Firstly, even though we have considerable knowledge on the subject of phylogenetics, new ideas are constantly emerging and we are still in the learning-phase with respect to its methodologies and the interpretation of results. Secondly, we are still in the process of developing a definition for a fungal species and how to recognize this unit. Although we have attempted to address the taxonomic status and reproductive mode of isolates residing in F. subglutinans sensu stricto, many questions remain unanswered. These include an understanding of how an asexual species should be defined, how many nucleotide differences constitute a species divergence in Fusarium and others. Our study and similar cases will thus represent an interesting topic for discussion as the fields of fungal reproduction and phylogenetic taxonomy advance.
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FOOTNOTES |
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Accepted for publication April 28, 2002.
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LITERATURE CITED |
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