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Published online 20 May 2008
Published in Crop Sci 48:1203-1210 (2008)
© 2008 Crop Science Society of America
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Patterns of Diversity in Populations of the Turfgrass Pathogen Colletotrichum cereale as Revealed by Transposon Fingerprint Profiles

Jo Anne Croucha, Bernadette M. Glasheena, Wakar Uddinb, Bruce B. Clarkea and Bradley I. Hillmana,*

a Dep. of Plant Biology and Pathology, Rutgers Univ., New Brunswick, NJ 08901-8520
b Dep. of Plant Pathology, The Pennsylvania State Univ., University Park, PA 16802

* Corresponding author (hillman{at}aesop.rutgers.edu).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Anthracnose disease of cool-season turfgrasses, caused by the fungus Colletotrichum cereale, has recently emerged as one of the most significant pathogens of Poa annua. Here we investigated the utility of four repetitive transposable elements as molecular markers for the analysis of C. cereale populations. Southern blot hybridization analysis revealed lineage-specific polymorphisms and distribution patterns for these transposons. Comparative phylogenetic analysis of three nonrepetitive protein coding DNA sequences against the transposon restriction fragment length polymorphisms indicated that the transposon sequences have similar evolutionary histories to those found in the sampled C. cereale population, despite the alteration of several transposon copies by repeat-induced point mutation. The variability and ubiquity of the Ccret2A15 transposon in C. cereale genomes suggest that this element could be used as a reliable DNA marker to discriminate between lineages of the fungus, identify hybrid genotypes, and analyze genetic diversity in populations of this turfgrass pathogen.

Abbreviations: ITS, intergenic transcribed spacer • kb, kilobase • PCR, polymerase chain reaction • RAPD, randomly amplified polymorphic DNA • RFLP, restriction fragment length polymorphism • RIP, repeat-induced point


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
DURING THE PAST DECADE, the anamorphic fungus Colletotrichum cereale sensu lato Crouch, Clarke and Hillman (formerly C. graminicola G.W. Wilson) (Crouch et al., 2006) emerged from relative obscurity to become one of the most devastating pathogens of the cool-season turfgrass Poa annua, causing epidemics of anthracnose disease in stands of this grass maintained as golf course greens in North America (Smiley et al., 2005) and the United Kingdom (Mann and Newell, 2005). For golf course superintendents, management of anthracnose is a challenging and expensive undertaking. Control of the disease relies heavily on fungicide applications; however, resistance to benzimidazole, strobilurin, and sterol inhibitor fungicidal chemistries is an increasingly widespread phenomenon (Avila-Adame et al., 2003; Crouch et al., 2005; Wong and Midland, 2007; Wong et al., 2007; B.B. Clarke, unpublished data).

Because genetic variability between isolates of C. cereale may influence the trajectory of anthracnose disease of turfgrass, a comprehensive understanding of how C. cereale populations are organized and distributed across their geographic range could enhance the development and implementation of effective disease management strategies. At present only limited population-level data, derived from randomly amplified polymorphic DNA (RAPD) or isozyme markers, are available for the fungus (Backman et al., 1999; Browning et al., 1999; Chen et al., 2002; Horvath and Vargas, 2004), although two major lineages, designated clades A and B, have been recognized on the basis of intergenic transcribed spacer (ITS) nucleotide sequences (Crouch et al., 2005) and a multiple gene genealogical approach (Crouch et al., 2006). Currently, few apparent biological patterns are readily ascribable to this divergence, and uncertainty exists as to whether the two groups are genetically isolated. Colletotrichum cereale clades A and B are morphologically indistinguishable and have overlapping distributions; furthermore, each lineage includes a cohort of both disease-inducing isolates from turfgrass species and their nonpathogenic counterparts from cereal crops and natural grassland ecosystems (Crouch et al., 2006; J.A. Crouch and B.I. Hillman, unpublished data).

The presence or absence of transposons at particular loci is a major contributor to restriction fragment length polymorphism (RFLP) variation in filamentous fungi. The primary objective of this research was to determine if repetitive transposable elements from the C. cereale genome could be developed as molecular markers to assess population structure and variability in the species. In the present study, we evaluated four elements representing three species of transposons (Crouch et al., 2008) from C. cereale as molecular markers to examine population structure in this organism. Because of their ubiquitous and repetitive nature, molecular marker systems based on mobile transposable element polymorphisms have been used for population-level analyses of numerous organisms, including several filamentous fungi (Diez et al., 2003; Farman et al., 1996; Girard and Freeling, 1999; Kohn et al., 1991; Linder-Basso et al., 2001; Milgroom et al., 1992). The presence of a transposon at a genomic locus is typically a good indicator of identity by descent, while the absence of an element at a site is recognized as the ancestral state. Transposon insertional RFLP data can be relatively free of homoplasic data that might be inconsistent with an organism's evolutionary history, since the independent insertion of two different transposon copies at the exact same location on a chromosome is extremely unlikely. The parallel loss of transposon copies through excision or homologous recombination may be problematic, however (Carbone et al., 1999), and alteration by repeat-induced point (RIP) mutation of transposons may complicate the evolutionary signal (Crouch et al., 2008). Although base substitutions in the restriction enzyme recognition sequence can theoretically generate nonhomologous bands of identical size, there is little likelihood of this type of convergence in groups of closely related individuals where evolutionary rates are low; in particular, parallel independent gains of restriction sites occur with only a small probability (Nei and Tajima, 1983; Nei and Tajima, 1985; Upholt, 1977).

The objectives of this study were to determine if transposon RFLP markers support the separation of C. cereale into two distinct lineages as previously described (Crouch et al., 2005, 2006) and to examine whether these markers offer any advantages over nucleotide sequence data in discerning structure in C. cereale populations. In particular, we considered to what extent these transposons could extend our understanding of how the major C. cereale lineages have evolved.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Fungal Cultures
Twenty-one single spore cultures of C. cereale were isolated from diseased Poa annua on 11 golf course greens located within a 100-km radius in Pennsylvania (Fig. 1 , Table 1 ) and cultured as previously described (Crouch et al., 2006). Isolates of C. graminicola from Zea mays, C. sublineolum from Sorghum bicolor, and C. falcatum from Saccharum officinarum were used for outgroup comparisons.


Figure 1
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  		Figure 1. Map of Pennsylvania, illustrating the origination of the Colletotrichum cereale isolates used in this study. The number of isolates from each location is listed in parentheses after the location name.

 

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  		Table 1. Fungal strains used in this study. All fungi were isolated from Poa annua unless otherwise noted.

 
RFLP Analyses
Genomic DNA was isolated from mycelia using a standard phenol:chloroform extraction protocol (Sambrook and Russell, 2001). HindIII-digested genomic DNA was size fractionated by gel electrophoresis for 18 h at 45v in 1x TBE buffer, then visualized using ethidium bromide staining. Southern blots for RFLP analysis were prepared by transferring the DNA to Zeta-Probe membranes (Bio-Rad, Hercules, CA) using a Posiblot Pressure Blotter (Strategene, La Jolla, CA) at 75 mm Hg. Five hundred nanograms of polymerase chain reaction (PCR) amplicon from each of the four individual transposon sequences (Table 2 ) were radiolabeled with [{alpha}32P]dCTP (MP Biomedicals, Irvine, CA) using the Random Primers DNA Labeling System (Invitrogen Corp., Carlsbad, CA). Hybridizations were performed as previously described (Crouch et al., 2008). Hybridized membranes were exposed to autoradiography film (Lab Scientific, Inc., Livingston, NJ) in the presence of an intensifying screen and incubated at –70°C for 24 to 48 h before development. We evaluated RFLP banding patterns of four sequences from three transposon species (Collect1I29, Ccret1DBP6, Ccret2DBP16, and Ccret2A15).


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  		Table 2. Primer sequences used in this study.

 
Because the retrotransposon sequences Ccret1DBP6 and Ccret2A15 were identified in all of the C. cereale isolates sampled, the RFLP patterns from these elements were used to discern patterns of population subdivision. Bands on the autoradiograms were scored visually as either present or absent and coded as binary data. The datasets were analyzed to identify population groupings using the Bayesian Monte Carlo Markov chain-based clustering program Structure 2.1 (Falush et al., 2003; Pritchard et al., 2000) for 1,000,000 repetitions each, with the first 20,000 discarded as burn-in. These analyses were run using the admixture model and correlated allele frequencies between populations, which is considered the best strategy for detecting subtle differences in population structure (Falush et al., 2003). The degree of {alpha} admixture was empirically derived from the data, and the distribution of allelic frequencies {lambda} was set to 1 (Falush et al., 2003). Twenty runs were performed for K = 1 through 10 (where K = the maximum number of populations).

Phylogenetic Analyses
Phylogenetic analysis was performed using three nuclear loci previously shown capable of differentiating between the two major lineages of C. cereale, with PCR amplified fragments of the ITS1/5.8S/ITS2 ribosomal DNA (ITS), the HMG-box of the Mat-1-2 mating idiomorph (HMG), and the manganese superoxide dismutase (Sod2) genes used to generate nucleotide sequence data as previously described (Crouch et al., 2006). The sister species of C. cereale—C. sublineolum and C. falcatum—along with the more distantly related species, C. graminicola (Crouch et al., 2006; J.A. Crouch and B.I. Hillman, unpublished data) were included as outgroup taxa. Multiple sequence alignments were constructed using Clustal W (Thompson et al., 1994) as launched in MegAlign (DNASTAR, Inc., Madison, WI), and manually adjusted to exclude gaps and ambiguously aligned regions from the dataset. Tree topologies were estimated from the combined multilocus nucleotide sequence dataset in MrBayes v.3.1 (Huelsenbeck and Ronquist, 2003) by performing two simultaneous runs of one cold and three heated Metropolis-coupled Monte Carlo Markov chains (MCMCMC) for 40,000,000 generations and sampling trees every 500 generations. Each individual gene region was partitioned in the analysis, and a general evolutionary model for each partition was incorporated as selected using the program ModelTest v.3.06 (Posada and Crandall, 1998) (ITS model: TrNef+G, A->G 1.5282, C->T 3.9607; {alpha} = 0.1317; HMG model: HKY+G, A = 0.2654, C = 0.2953, G = 0.2622, T = 0.1770; Ti/Tv = 1.2783; {alpha} = 1.50421; Sod2 model: TrN+I, A = 0.2477, C = 0.3035, G = 0.2612, T = 0.1876; A->G 5.0186, C->T 4.8842, G->T 1.0; Pinv = 0.4998; equal rates for all sites). Run diagnostics were performed every 1000th generation, with the first 25% of the output discarded as burn-in. To confirm that the two separate runs converged to a stationary distribution, the average standard deviation of split frequencies, the potential scale reduction factor convergence diagnostic, and the plot of generation versus log likelihood were each examined for values and distributions characteristic of samples drawn from a posterior probability distribution. Trees sampled from the posterior distribution were imported into PAUP* v.4.0b10 (Swofford, 2000) and used to construct 75% majority-rule consensus trees.

Nucleotide Sequences
All new sequences generated by this study have been deposited in the National Center for Biotechnology Information GenBank database (accession numbers DQ663514–DQ663534).


   RESULTS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Phylogenetic Assessment of Populations Using Sequence Data
Although drawn from a geographically limited region in Pennsylvania, the fungal specimens included in this study represent both of the major C. cereale evolutionary lineages, clades A and B, allowing us to test whether the multilocus RFLP banding patterns of four sequences from three transposon species (Collect1I29, Ccret1DBP6, Ccret2DBP16, and Ccret2A15) could be used to distinguish the major lineages in this species, even on a relatively fine scale. Three of the probes—Collect1I29, Ccret1DBP6, Ccret2DBP16—have been altered in the past through RIP mutation, a genome defense system deployed by filamentous fungi that produces C->T and G ->A transitions in repetitive DNA (Cambareri et al., 1989), including transposable elements. To evaluate the transposon-based population hypotheses, a strict consensus tree of 21 C. cereale isolates was constructed from 33,206 trees using Bayesian estimates from the combined ITS/HMG/Sod2 dataset (Fig. 2 ). Both lineages were represented in the tree topology and supported by posterior probabilities of 100, with 13 isolates from C. cereale clade A and 8 isolates from clade B. Two of the geographic locations contained isolates from each of the two clades.


Figure 2
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  		Figure 2. Multilocus tree estimated through Bayesian phylogenetic analysis of three protein coding genes supporting the division of the Colletotrichum cereale isolates into two main lineages, clades A and B (–ln likelihood = 3430.89).

 
Limited Distribution of the TE Sequences Collect1I29 and Ccret2DBP16
The TE markers Collect1I29 and Ccret2DBP16 produced fingerprint profiles largely consistent with the phylogenetic groups and confirmed the repetitive nature of the transposon sequences when hybridized against the restricted DNA gel blots. Isolates phylogenetically characterized as C. cereale clade B resulted in ~25 hybridizing bands on the autoradiograms (Fig. 3 ) with little polymorphism observed between the individual isolates. In contrast, all clade A isolates except PA-50183 were devoid of the Collect1I29 and Ccret2DBP16 sequences, as were the outgroup samples of C. graminicola and C. sublineolum. Polymerase chain reaction amplification using several alternate primer pairs from Collect1I29 and Ccret2DBP16 recovered the same pattern of presence or absence, failing to yield a product in clade A isolates even under conditions of low stringency (data not shown). The presence of these two elements in the genomes of C. cereale clade B and not in clade A is consistent with the fact that both of these transposon sequences are extensively RIP mutated, a process that has not been observed for clade A strains of the fungus (Crouch et al., 2008). But the PCR-based identification of Ccret2DBP16 from two of the three C. falcatum outgroup strains (data not shown) suggests that this RIP-mutated element was already present in the common ancestor of C. falcatum and C. cereale and was subsequently lost from C. cereale clade A after its divergence from clade B (Fig. 4 ).


Figure 3
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  		Figure 3. Southern blot hybridizations of HindIII-digested genomic DNA from a representative sample of Colletotrichum cereale clade A and B isolates using four transposon sequences as the probe. (A) Collect1I29 DNA transposon, (B) Ccret1DBP6 retrotransposon, (C) Ccret2DBP16 retrotransposon, (D) Ccret2POL2/3 (from clone A15) retrotransposon.

 

Figure 4
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  		Figure 4. A schematic tree showing the presence or absence of the transposons evaluated in this study. (RIP = repeat-induced point.)

 
The Retrotransposons Ccret1 DBP6 and Ccret2 A15 Are Found in Both C. cereale Lineages
In contrast to the limited distribution of Collect1I29 and Ccret2DBP16 within the species, Southern blot analysis of the C. cereale population (Fig. 3) using the RIP-mutated Ccret1DBP6 probe revealed the presence of this retrotransposon in both of the major C. cereale lineages, although PCR amplification using a range of high and low stringency conditions and primer pairs demonstrated that Ccret1DBP6 was absent from the DNA of C. graminicola, C. sublineolum, and C. falcatum (data not shown). Each of the C. cereale clades exhibited visually distinct banding patterns. Clade B isolates yielded between 9 and 15 Ccret1DBP6 bands ranging in size from ~0.5 to 9 kilobase (kb), but with the exception of isolate PA-50183, the clade A isolates faintly hybridized at only one or two restriction fragments. Low copy number of Ccret1DBP6 in the genome of clade A isolates was anticipated since analysis of the element from a cosmid library found that this retrotransposon is present only as two unmutated copies at a single genomic locus in clade A isolate NJ-6340 (Crouch et al., 2008). The observed faint hybridization to the RIP-mutated probe sequence was similarly predicted from the cosmid sequence data since this transposon was not found to be RIP-mutated in clade A (Crouch et al., 2008). All C. cereale isolates shared the 1-kb Ccret1DBP6 band, indicating that this is probably the ancestral locus of Ccret1DBP6 and that subsequent amplification and RIP-mutation of this retrotransposon occurred only after the divergence of clades A and B (Fig. 4).

The Ccret2A15 retrotransposon sequence was the only transposon used as a probe in this study that was not RIP-altered, although in clade B strains of the fungus, this element can be present as both RIPped and non-RIPped variants within a single genome (Crouch et al., 2008). Of the four sequences evaluated, Ccret2A15 was the only transposon that produced a polymorphic RFLP banding pattern (Fig. 3). Like the other three transposon probes, the Ccret2A15 marker produced a visually distinctive banding pattern clearly differentiating between isolates belonging to phylogenetic clades A and B. Likewise, clade A isolate PA-50183 exhibited the clade B-like fingerprint rather than the clade A-like pattern predicted by phylogenetic affiliation. Polymerase chain reaction amplification identified Ccret2A15 from one of the two C. sublineolum isolates and all three of the C. falcatum isolates; however, it was absent from the more distantly related C. graminicola, suggesting that this transposon sequence was present in the common ancestor of C. cereale, C. sublineolum, and C. falcatum (Fig. 4).

Estimates of Population Subdivision Using the Retrotransposon RFLP Datasets
Since the Ccret1DBP6 and Ccret2A15 sequences were present in all of the C. cereale isolates sampled for this study, binary datasets were generated by coding the banding patterns produced by these elements as either present or absent to evaluate population subdivision. We first used the binary datasets to determine if the retrotransposon distribution within the genome was congruent with the HMG/ITS/Sod2 evolutionary hypothesis. Consistent with the phylogenetic tree topology and the visual estimations made from the autoradiograms, two distinct populations, corresponding to clades A and B, were inferred from the RFLP datasets using the Bayesian clustering method implemented in the program Structure (Pritchard et al., 2000).


   DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Consistent with the multilocus phylogenetic tree topology (Fig. 2), all four transposon RFLP fingerprint patterns recovered the division of C. cereale into two main lineages as previously established for the species (Crouch et al., 2006), either through distinct banding patterns or by their presence or absence. The only inconsistency observed between the nucleotide sequence data set and the transposon RFLPs was the manifestation of clade B-like banding patterns for the clade A isolate PA-50183 by all four transposon markers (Fig. 4), suggesting that this isolate may be a hybrid between the two lineages. Despite the potential for RIP-induced homoplasy in these analyses (Crouch et al., 2008), our data showed the C. cereale transposon RFLP signal in these analyses to be largely congruent with the non-TE datasets, with both the RFLPs and sequence analysis of three protein-coding genes yielding the same general conclusions. Although none of the RFLP fingerprints predicted any further population substructure beyond the two main lineages, this is likely a reflection of the small, geographically limited sample size evaluated in this study rather than a lack of sensitivity on the part of the markers. Since the purpose of this study was to determine whether transposon RFLP patterns are suitable molecular markers rather than drawing conclusions about the genetic makeup of populations, further study will be required to make this determination.

The interspecific distribution and intraspecific polymorphic banding patterns demonstrated that of the four markers evaluated, Ccret2A15 sequence has the potential to serve as an effective RFLP marker for future population analysis of C. cereale and may even be adopted for use in populations of the closely related, economically important plant pathogens C. sublineolum and C. falcatum. Ccret2A15 is polymorphic and was present in all C. cereale isolates sampled in this study; additionally, PCR-based screening shows that this transposon is widely distributed across the geographic range for this species and is present in both turfgrass pathogenic strains as well as C. cereale isolated from prairie, forage, and cereal crops (J.A. Crouch and B.I. Hillman, unpublished data). In contrast, while any of the other three transposons surveyed in this work—Collect1I29, Ccret1DBP6 and Ccret2DBP16—might in theory be used to evaluate populations of C. cereale clade B given the polymorphic banding patterns shown by the group, the high level of RIP mutation that characterizes these elements renders the use of these transposons as RFLP markers potentially problematic (Crouch et al., 2008). Under normal circumstances, although base substitutions in a restriction enzyme recognition sequence can theoretically generate nonhomologous bands of identical size, there is little likelihood of this type of convergence in groups of closely related individuals where evolutionary rates are low; in particular, parallel independent gains of restriction sites with six-base recognition sequences are have been found to occur with only a small probability (Nei and Tajima, 1983, 1985; Upholt, 1977). But for RIPped transposons, restriction sites are more rapidly gained or lost since overall nucleotide composition and dinucleotide patterns are skewed, often occurring at a range of different levels contingent on how many rounds of RIP mutation have acted on a given element. Thus, because RIP mutation has been found to act on these transposons, we cannot exclude the possibility that the different allelic states (±) observed at each locus are merely artifacts of RIP alterations rather than accurately reflecting common descent. For these reasons, for C. cereale clade B and other fungi where there is evidence of RIP mutation, transposon RFLP datasets should be regarded as potentially homoplasic unless independently derived support exists for the interpretation of homology. In the present study, however, the agreement between transposon RFLP data and the three independent protein coding genes attest to the consistency of the RFLP data in this sampled population and suggest that the Ccret2A15 transposon-based marker can serve as a valuable tool in future population studies of C. cereale.


   ACKNOWLEDGMENTS
 
We thank Lisa Vaillancourt for providing the Colletotrichum graminicola and C. sublineolum cultures and the National Institute of Agrobiological Sciences Genebank of Ibaraki, Japan, for the C. falcatum cultures used in this study. This work was funded by grants from the Rutgers Center for Turfgrass Science to B.I.H. and B.B.C. and by the New Jersey Agricultural Experiment Station. We gratefully acknowledge financial support for J.A.C.'s graduate studies provided by a U.S. Environmental Protection Agency Science to Achieve Results (STAR) Graduate Fellowship, the Ralph Geiger Endowment, a Rutgers Excellence Fellowship, the Robert White-Stevens Fellowship, the Peter Selmer Loft Memorial Scholarship fund, and a Land Institute Natural Systems Agriculture Graduate Fellowship. Although the research described in this article has been funded in part by the USEPA's STAR fellowship program through grant FP-91652101, it has not been subjected to USEPA review and therefore does not necessarily reflect the views of the agency, and no official endorsement of any products or commercial services mentioned in this article should be inferred.


   NOTES
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ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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Received for publication August 2, 2007.


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