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Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131
David J. Jacobson
Department of Biological Sciences, Stanford University, Stanford, California 94305
Laura Salter
Department of Mathematics and Statistics, University of New Mexico, Albuquerque, New Mexico 87131
Donald O. Natvig 1
Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Although species of Neurospora are among the most studied model organisms in genetics and biochemistry, basic questions remain with respect to their ecology and population biology. In this study, we sought to clarify relationships among individuals over a small spatial scale, toward assessing both local variation and mode of colonization. Isolates of Neurospora were collected after fires in the Florida Everglades (May 1999), where abundant colonies appeared on diverse plants, including grasses and woody shrubs. Colonies were sampled in a linear fashion from two adjacent scorched sugarcane stems at one site and from a burned woody shrub at a distant second site. Species and mating types were assigned based on crossing behavior. Variation at two loci, het-c and frq, was determined by direct sequencing of PCR products. The results demonstrated substantial within- and among-species variation on a small scale, with up to three species and six different haplotypes occurring on a single stem. In total, four species and more than 10 genetically distinct individuals (haplotypes) were present across the three stems, often with multiple individuals occupying the same position. A permutation analysis revealed that individuals were not distributed randomly and that adjacent nodes on cane stems were more likely than chance to be colonized by the same haplotype. This suggests that visible eruptions of conidia on burned plants reflect substantial vegetative mycelial spread through subsurface tissues after primary colonization. Results also revealed that adjacent isolates from a single plant can possess different functional alleles at het-c, an observation meaningful in the context of the proposed role of het-c in self recognition.
Key words: clonal and vegetative growth, colonization, ecology, het-c
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Jacobson et al unpubl). Studies with these isolates have been fruitful in developing an understanding of species distribution on a global scale. On a local scale, studies have shown that multiple genetically distinct individuals of the same species and even members of different species can be found in a given location (Perkins et al 1976, Perkins and Turner 1988). However, the magnitude of variation in a given location has not been quantified and mechanisms of colonization and dispersal remain issues of debate.
Most field collections of Neurospora species have been from tropical and subtropical regions after either planned or natural fires, and natural populations of Neurospora often occur where fire is a part of the ecosystem (Perkins et al 1976, Perkins and Turner 1988, Pandit and Maheshwari 1996, Turner et al 2001). Current evidence suggests that most Neurospora species respond dramatically to fires. Germination of ascospores (sexual propagules) requires either direct heat activation or activation by chemical byproducts in burned plant material (Perkins 1986, Pandit and Maheshwari 1996). In addition, fire appears to create ideal substrate conditions, in the form of scorched, dead plant material, for colonization.
The extent of colonization of burned plants by species of Neurospora can be visually impressive. Within 2 wk of the Florida Everglades fires in spring 1999, conidiating species of Neurospora were observed in some places on nearly all plants, from grasses to woody stems (Jacobson and Natvig, pers obs). For instance, in a single 1000 m2 area, it was possible to observe thousands of eruptions (tufts of mycelia and conidia, Fig. 1) on burned stems.
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Neither hypothesis has received absolute support in previous studies. There are reports of multiple species and mating types from a single plant and, occasionally, from a single eruption (Perkins et al 1976, Perkins and Turner 1988, Turner et al 2001). On the other hand, there is evidence that colonization of plant stems by a single individual can lead to the copious spread of mycelium below surface tissues (Fig. 1; Pandit and Maheshwari 1996), leading to the eruption of hyphae and conidia in multiple locations on the same substrate. The abundance of conidia produced by species of Neurospora further suggests the possibility of dispersal of individuals by wind and animals, but the extent of propagation by these mechanisms is not known.
The present study examined relationships among conidial isolates of Neurospora sampled from stems at two locations, toward the goals of testing these hypotheses and obtaining preliminary information regarding population structures. Isolates were characterized in terms of species and mating types, as well as by sequence analysis of two autosomal loci, frq and het-c, both of which have proven valuable for typing individuals in previous studies (Gallegos et al 2000, Powell et al 2001). The results demonstrate colonization of single stems by multiple individuals and species, with a minimum of 10 individuals and four species being observed across three stems, refuting the hypothesis that growth on individual stems represents clonal propagation only. The spatial distribution of individuals on stems nevertheless provides evidence that the subepidermal spread of mycelium and possibly dispersal by conidia contribute to observed patterns of colonization. The complex mosaic of species and individuals observed at local sites confirms that species of Neurospora are excellent candidates for studies of fungal population biology and ecology.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In the notation used here, relative sampling positions are indicated with numbers after hyphens. So, for example, SC1-2 refers to an isolate from the second node of sugarcane stem No. 1, while Sh-1 refers to an isolate from the first (lowermost) sample point on the shrub. Details regarding the positions at which isolates were collected are presented in Tables I and II.
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, Turner et al 2001). In the laboratory, a small section (approximately 10 mm2) of each filter-paper strip was removed with sterile scissors and placed on agar medium to produce a primary culture. All cultures first were tested for self-fertility on Westergaard's synthetic crossing medium (Davis and de Serres 1970). Self-fertile strains with four-spored asci were assigned to N. tetrasperma, a self-fertile member of the genus. Primary cultures producing eight-spored asci were presumed to harbor mixed cultures (i.e., with both mat A and mat a mating types), representing any of the heterothallic species, N. crassa, N. intermedia, N. discreta or N. sitophila. Mixed-mating-type cultures were resolved by dilution plating to recover single-conidium isolates. Self-sterile isolates obtained in this manner were crossed against designated species tester strains and assigned to species based on fertility (Perkins and Turner 1988).
Sequence analysis of frq and het-c –
Nucleotide sequence data from two loci, frq (linkage group VII) and het-c (linkage group IIL), were obtained to assess within- and between-species variation. The molecular analysis of both loci was carried out by polymerase chain reaction (PCR), followed by direct sequencing of PCR products. Genomic DNA was isolated as previously described (Gallegos et al 2000). For each isolate, an upstream region of the frq gene and a portion of the het-c coding region were amplified using standard PCR methods. PCR products were prepared for direct dideoxy sequencing with Amicon® Microcon®-PCR Centrifugal Filter devices, following the manufacturer's specifications. Nucleotide sequence data for purified PCR fragments were obtained with dideoxy dye-terminator chemistry (ABI Prism® BigDyeTM Terminator Cycle Sequencing Ready Reaction Kit with AmpliTaq® DNA polymerase, FS) and a model 377 automated sequencer, in accordance with instructions supplied by the manufacturer (Perkin-Elmer). Raw nucleotide sequence data were processed and analyzed with the SequencherTM (version 3.1.1) software package and ClustalW (Thompson et al 1994). Final alignments were obtained by visual inspection as described below.
In species of Neurospora, frq has a key role in control of the circadian cycle (Dunlap 1999). Previous studies demonstrated that sequences in the frq upstream region show substantial polymorphism, even among closely related individuals of the same species (Gallegos et al 2000). The target region of frq was amplified with primers 5' CAA TAC CTC TCC TCC TCC CTA C 3' and 5' CTC TGC TGC TAG TAT CTC GC 3'. With respect to the N. crassa GenBank entry (accession number U17073), these primers correspond to nucleotides 809–830 and 1561–1542, respectively. The PCR fragment produced with this primer pair is 752 nucleotides in length. Purified PCR products were sequenced with the primers above and a third primer, corresponding to nucleotides 1271–1252.
The het-c locus likewise has proven useful in distinguishing among individuals of the same species (Powell et al 2001). This locus is of additional interest in population studies because it is a heterokaryon incompatibility gene that is involved in self recognition (Wu et al 1998). The importance of self recognition in nature is a function of the frequency at which individuals with different functional het alleles encounter one another. Our sampling permitted assessment of the het-c status of adjacent isolates from a single plant.
For each isolate, the specificity region (Saupe et al 1996) of the het-c locus was amplified, along with flanking regions, as an approximately 300 base-pair PCR product, with the exact product size being a function of the specific allele amplified. The N. crassa het-cOR sequence (strain 74-OR23-IVA, GenBank accession number L77234, Saupe et al 1996) served as template for the design of primers: 5' CAG TGG CTC TCG TGG CAG AGG 3' and 5' GGC CAA CGA TCA CTT CAC CCA AT 3', which correspond to nucleotides 1153–1173 and 1463–1441, respectively. Nucleotide sequence data for the het-c purified PCR products were generated with the primers used for amplification.
The partial frq and het-c sequences reported here have been deposited with GenBank under accession numbers AY091529–AYO91548 and AF494255–AF494274, respectively.
Tree-building methods –
Phylogenetic trees were constructed to determine whether mating behavior accurately reflected phylogeny. Analysis of het-c in the context of phylogeny is complicated by the fact that this locus is under balancing selection, with multiple ancient alleles maintained in populations. The expectation is therefore that speciation will be reflected in het-c trees but only within functional allele classes (Powell et al 2001).
Final nucleotide sequence alignments for frq and het-c were obtained manually. The frq alignment was straightforward, with homologous nucleotide positions being unambiguous for all sequences. No insertion-deletion events were observed. In addition to sequences obtained for this study, a partial N. crassa frq sequence was included in the alignment (Oak Ridge background, accession number U17073, Aronson et al 1994). The resulting alignment included residues corresponding to nucleotides 878–1242 in the N. crassa Oak Ridge frq sequence.
The het-c nucleotide sequence alignment was informed by the het-c amino-acid sequence alignment of Wu et al (1998). In addition to the sequences reported here, these partial het-c nucleotide sequences were included in this alignment (GenBank accession numbers given in parentheses): N. crassa Oak Ridge allele from strain 74-OR23-IVA (L77234), N. crassa Groveland allele from strain Groveland 1-c (AF196305), N. crassa Panama allele from strain c9-2 (AF195874), N. tetrasperma Oak Ridge alleles from strains P514a and P556a (AF195261 and AF195265, respectively), N. tetrasperma Panama allele from strain P586a (AF195271), and N. tetrasperma Panama variant allele from strain P535a (AF195263). The resulting alignment included residues corresponding to nucleotides 1230–1434 in the entry for the N. crassa Oak Ridge (het-cOR) allele.
Maximum-likelihood and parsimony methods were employed to estimate relationships among isolates at frq and het-c loci, using the beta 8 version of PAUP* 4.0 (Swofford 2001). Bootstrap analyses were performed using 1000 bootstrap replicates.
Haplotype distribution – A permutation procedure was developed to test whether identical haplotypes were present at adjacent nodes more frequently than expected by chance. Only data for the cane stems were employed in obtaining the results presented. Results obtained with data pooled across sites were congruent with those presented, but they were excluded here due to concerns that differences in genetic structure between sites might lead to artificial clustering of haplotypes. To perform the test, the haplotype data were permuted 1000 times by randomly assigning haplotypes to stem locations. For each permutation, the number of times that identical haplotypes occurred at adjacent nodes was recorded. The test was performed for isolates of all species on cane combined and separately for isolates of N. tetrasperma only. It was not performed for individual species other than N. tetrasperma due to small sample sizes. The field data revealed four instances where identical haplotypes occurred at adjacent cane nodes, considering isolates of all species, and three instances where identical N. tetrasperma haplotypes occurred at adjacent cane nodes. Therefore, in the all-species permutation test, a P-value was computed using the percentage of replicates that showed four or more adjacent positions with identical haplotypes, while in the N. tetrasperma test, a P-value was computed using the percentage of replicates that showed three or more adjacent positions with identical haplotypes. All computations for permutation testing were carried out with programs written by one of the authors (L.S.) in the S-Plus software package (version 5.0, MathSoft Inc., 1998). Details regarding implementation of the test are presented below.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Laboratory tests for self fertility and crossing experiments against standard Neurospora tester strains demonstrated that four different species of Neurospora were present among the samples taken from the three plants. Eleven of the 20 isolates examined were self-fertile N. tetrasperma, six were N. sitophila, two were N. crassa and one was N. intermedia (Table I).
Five of the six N. sitophila isolates were mating type mat A, while the sixth isolate was mat a. One of the two N. crassa isolates was mat a, while the second was mat A. The sole N. intermedia isolate was mat A.
Sequence variation at frq and het-c –
Substantial variation was observed among isolates for both frq and het-c (Figs. 2 and 3). Among the 20 isolates, there were four different frq variants and seven het-c variants. Variation at frq supported species assignments based on crossing behavior (Fig. 2). Variation at the het-c locus included ancient functional allelic diversity, with each variant falling into one of two previously recognized het-c functional allele groups, Panama (het-cPA) or Oak Ridge (het-cOR). The distinct functional alleles observed at this locus diverged prior to the origin of the genus and family (Wu et al 1998; Table I; Fig. 3). Closely related individuals of the same species can have the same or different functional alleles at het-c. This has been shown previously (Powell et al 2001) and was observed here as well. For example, N. tetrasperma isolate SC2-18 features the Oak Ridge functional allele (het-cOR) while N. tetrasperma isolate SC2-15 has the Panama functional allele (het-cPA). Within het-c Panama and Oak Ridge functional allele classes, each variant was specific for a particular species, and relationships among variants reflected species assignments (Fig. 3), providing additional support for these assignments.
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Isolates examined from the two cane stems included three different species and eight different haplotypes. Three different species and four distinct haplotypes were present among the shrub stem isolates, which were sampled at 30 cm intervals. The pattern of haplotype distribution suggests a combination of colonization by multiple ascospore-derived individuals and vegetative spread on individual stems. For example, one sugarcane stem showed N. tetrasperma at neighboring nodes (SC1-6, haplotype 6; SC1-7, haplotype 1) and at a non-neighbor node (SC1-11, haplotype 4). N. sitophila occurred at neighboring nodes SC1-9 (haplotype 2) and SC1-10 (haplotype 2) and also at node SC1-13 (haplotype 5) (Tables I and II). The second cane stem, adjacent to the first, featured N. tetrasperma at several pairs of neighboring nodes: SC2-2 (haplotype 3) and SC2-3 (haplotype 3) near the base of the stem, SC2-10 (haplotype 1) and SC2-11 (haplotype 1), and SC2-14 (haplotype 4) and SC2-15 (haplotype 4), with the latter two pairs located in the upper third of the stem (Table I). N. crassa was collected at nodes SC2-6 (haplotype 7) and SC2-16 (haplotype 8) from the same stem. N. tetrasperma again was sampled at the top of this stem, at node SC2-18.
Conidial eruptions on stems signal mycelial growth below surface tissues (Fig. 1), raising the question of how much stem volume may be occupied by a single individual. In the case of the shrub stem, four different individuals were recovered at sampling points separated by 30 cm intervals. However, the several instances of adjacent cane nodes possessing identical haplotypes (Table II) suggested vegetative spread of single individuals through subepidermal tissues.
To assess the likelihood that such observations actually indicate vegetative spread of a single individual, permutation analyses were performed using the haplotype data obtained from the cane isolates (see Materials and Methods). Considering all cane isolates, identical haplotypes occurred at adjacent positions four times out of nine instances where adjacent nodes were sampled (Table II). Permutation analysis demonstrated that the occurrence of four or more pairs of neighboring nodes with identical haplotypes was a rare event, with 11 instances of four and one instance of five such node pairs in 1000 replicates (Fig. 4A). Therefore, the occurrence of identical haplotypes at adjacent positions four times out of nine instances where adjacent nodes were sampled is highly significant (P = 0.012). Likewise, when considering only the 10 N. tetrasperma isolates from cane, the corresponding permutation analysis produced 30 instances of three adjacent node pairs and one instance of four adjacent node pairs with identical haplotypes in 1000 replicates (Fig. 4B). Again, the actual finding of three instances with identical haplotypes out of four where neighboring nodes possessed N. tetrasperma was significant (P = 0.031), and it further suggests that haplotypes were non-randomly distributed in our samples.
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Ascospore dispersal cannot account for haplotype distributions in our samples because none of the observed colonies had produced perithecia before sampling. As of yet, we cannot assess the likelihood of clonal spread between different plants by conidial dispersal.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). These results almost certainly understate the diversity present. More than half of the primary cultures were comprised of two or more individuals, and only a subset of these were analyzed after recovery of single-spore isolates (see Results). Furthermore, isolates were scored for only three genes. It is likely that different isolates with the same three-gene haplotype were not identical in all cases throughout their genomes, especially in cases where a given haplotype was observed at two different field sites.
Among sexual populations of filamentous fungi, there appears to be broad variation in the range of diversity that can exist in a given locale. The substantial within- and among-species variation observed here for Neurospora appears to parallel that observed for certain other fungi. Both ascomycetes and basidiomycetes, including Lophodermium piceae (Müller et al 2001), Rhabdocline parkeri (McCutcheon et al 1993), Coriolus versicolor and Stereum hirsutum (Boddy and Rayner 1982), have been shown to exhibit considerable variation on small scales. However, such variation stands in contrast to that observed for the basidiomycete Armillaria bulbosa. In one location, a single A. bulbosa genetic individual was estimated to be 1500 years old and occupied a 15-hectare region (Smith et al 1992).
Ecology and distribution –
Previous studies have resulted in several tentative conclusions relevant to the ecology of Neurospora species (Perkins et al 1976, Perkins and Turner 1988, Pandit and Maheshwari 1996, Turner et al 2001): (i) Conidia are not durable propagules. Their primary roles appear to be fertilization and perhaps dispersal of clones over limited spatio-temporal scales. (ii) Ascospores, in addition to being sexual propagules, are more durable than conidia and are present and abundant in some natural reservoir, probably soil, where they survive for long periods. (iii) Ascospores are dormant until activated by heat or exposure to chemical byproducts of burned vegetation. (iv) The ecological role of Neurospora species is that of primary colonizers in the succession associated with decomposition of plants.
Although our field observations are consistent with these conclusions, our specific observations on local distribution demonstrate a greater degree of intra- and interspecies variation than has been revealed in previous studies, highlighting a need for additional study on both large and small scales. Most notably, the occurrence of multiple species in single samples has been observed rarely (Perkins and Turner 1988) but was the rule among our Florida samples. Furthermore, the magnitude of species diversity observed in the Florida sample, four species among 20 isolates, might be exceptional. In any case, it appears to stand in contrast with recent studies of the genus in temperate western United States forests, where nearly 95% of 500 samples from New Mexico to Alaska appear to be N. discreta (unpubl).
Studies of natural isolates of Neurospora raise questions regarding within- and among-species competition. Under competitive exclusion (e.g. Hardin 1960), two species with identical ecological requirements cannot coexist indefinitely. It has been suggested that competitive exclusion does not hold for Neurospora species (Turner et al 2001) because there is no evidence that the different species of Neurospora in the habitats sampled either partition resources or exhibit differences in temporal or spatial distribution. The disturbed habitats inherent in causing Neurospora blooms are perhaps more consistent with nonequilibrium situations where species coexistence is influenced by environmental instability, such as in "lottery competition", where individuals compete for access to units of resources (Chesson and Warner 1981, Sale 1982), or in the "paradox of the plankton", where coexistence is present before competitive displacement can take place (Hutchinson 1961).
Pattern of substrate colonization and population structure –
It has been proposed that the primary colonization of a given plant by Neurospora occurs at the root, after the germination of ascospores in soil, with subsequent mycelial growth upward through root and subepidermal stem tissues (Pandit and Maheshwari 1996). The distribution of haplotypes observed on stems in our study strengthens the supposition that subepidermal mycelial growth is important in colonization. At the same time, the observed distribution is difficult to reconcile with the idea that all primary colonization takes place through root tissues. If colonization were strictly through root systems, then the observed presence of multiple haplotypes on a single stem would represent the growth of several individuals through the lower portions of the same stem. This mode of colonization would predict greater haplotype diversity on the lower portions of stems. No such pattern was observed. Dividing the sample points of each stem into root-proximal and distal halves, and considering position on a given stem only (i.e., excluding comparisons across different stems), seven haplotypes occurred only distally, six occurred only proximally and two occurred both proximally and distally (Tables I and II).
The high level of diversity observed among isolates in our study nevertheless suggests an important role for ascospores in colonization. Our results therefore are somewhat mysterious, given the presumption that the reservoir for ascospores is the soil. It is difficult to conceive rapid above-ground dispersal of ascospores from a soil reservoir in the hours and days after intense fire. It is possible therefore that conidia have an important role in the dispersal of individuals between stems. Additional study will be required to determine the relative roles of ascospores and conidia in colonization.
Questions regarding the mechanisms of colonization aside, it is clear that colonies of Neurospora in nature frequently encounter individuals of different species and different individuals of the same species. This would appear to provide ample potential for inter- and intraspecies interactions. Interspecies hybridization can be achieved with species of Neurospora in the laboratory (Perkins et al 1976, Turner et al 2001). The close association of isolates of different species in nature indicates the potential for hybridization in nature, but no evidence for such hybridization has been reported yet.
The observed close association of individuals also emphasizes the importance of heterokaryon incompatibility reactions among individuals. Heterokaryon incompatibility is believed to be important for nonself recognition, an argument supported by observed trans-species polymorphism at the heterokaryon incompatibity locus het-c (Wu et al 1998, Powell et al 2001). Our results show that neighbors on a single stem can possess different het-c functional alleles (Table I). Moreover, given the diversity of species in our sample, together with evidence that the genetics of heterokaryon incompatibility is conserved across species (Wu et al 1998, Powell et al 2001), it is reasonable to wonder if heterokaryon incompatibility genes have significance for interspecies interactions, in addition to intraspecies interactions. Evidence for both intraspecific and interspecific vegetative incompatibility reactions have been reported for another ascomycete genus, Phomopsis, which is associated with the inner bark of trees (Brayford 1990). It is not known to what extent het-c and other heterokaryon incompatibility genes in Neurospora function in interspecies interactions.
In summary, this study of Neurospora isolates from Florida demonstrates that (i) substantial diversity can be present among isolates on small scales, and (ii) the pattern of growth on a small spatial scale can derive from multiple ascospore-germination events combined with vegetative spread and perhaps dispersal by conidia. These observations represent pieces of a larger puzzle that is the natural history of this genus. Solving the larger puzzle will require additional study, which will include addressing questions in population biology and ecology. Such study holds great promise based on both the growing number of wild isolates obtained from natural settings (Turner et al 2001) and the long history of members of the genus in laboratory biology, including the recent acquisition of the genome sequence of N. crassa (http://www-genome.wi.mit.edu/annotation/fungi/neurospora/).
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Accepted for publication March 11, 2003.
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LITERATURE CITED |
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