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Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa
Paulette Bloomer
Department of Genetics, University of Pretoria, Pretoria, South Africa
Geoff S Ridley
New Zealand Forest Research Institute Ltd., Private Bag 3020, Rotorua, New Zealand
Michael J Wingfield
Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Armillaria root rot is a serious disease, chiefly of woody plants, caused by many species of Armillaria that occur in temperate, tropical and subtropical regions of the world. Very little is known about Armillaria in South America and Southeast Asia, although Armillaria root rot is well known in these areas. In this study, we consider previously unidentified isolates collected from trees with symptoms of Armillaria root rot in Chile, Indonesia and Malaysia. In addition, isolates from basidiocarps resembling A. novae-zelandiae and A. limonea, originating from Chile and Argentina, respectively, were included in this study because their true identity has been uncertain. All isolates in this study were compared, based on their similarity in ITS sequences with previously sequenced Armillaria species, and their phylogenetic relationship with species from the Southern Hemisphere was considered. ITS sequence data for Armillaria also were compared with those available at GenBank. Parsimony and distance analyses were conducted to determine the phylogenetic relationships between the unknown isolates and the species that showed high ITS sequence similarity. In addition, IGS-1 sequence data were obtained for some of the species to validate the trees obtained from the ITS data set. Results of this study showed that the ITS sequences of the isolates obtained from basidiocarps resembling A. novae-zelandiae are most similar to those for this species. ITS sequences for isolates from Indonesia and Malaysia had the highest similarity to A. novae-zelandiae but were phylogenetically separated from this species. Isolates from Chile, for which basidiocarps were not found, were similar in their ITS and IGS-1 sequences to the isolate from Argentina that resembled A. limonea. These isolates, however, had the highest ITS and IGS-1 sequence similarity to authentic isolates of A. luteobubalina and were phylogenetically more closely related to this species than to A. limonea.
Key words: Armillaria limonea, Armillaria luteobubalina, Armillaria novae-zelandiae, IGS-1, ITS, phylogeny, systematics
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Hood et al 1991, Kile et al 1991, Fox 2000). They also tend not to show a species-specific interaction with their hosts, although some species have defined host ranges (Termorshuizen 2000).
Armillaria species are known in many parts of the world and can be found on infected plants in temperate, subtropical and tropical regions (Hood et al 1991). Species associated with root rot are best known in Northern Hemisphere countries where considerable effort has been made to identify them. Armillaria root rot also has been recorded on various planted and natural hosts in South America and Indo-Malaysia, although little is known about the species occurring in these areas (Hood et al 1991). Many Armillaria species linked to outbreaks of the disease in South America are thought to be restricted to this area (Singer 1953, Kile et al 1994). Two species, A. novae-zelandiae (G.Stev.) Herink and A. limonea (G.Stev.) Boesew, are the exception in that they also have been reported in Australia and New Zealand (Ivory 1987, Hood et al 1991).
Little information is available regarding the identity of Armillaria in Indonesia and Malaysia (Hood et al 1991, Kile et al 1994). Reports of Armillaria in these regions are based mostly on the presence of the characteristic rhizomorphs or typical disease symptoms on infected trees (Kile et al 1994). In most reports from Indo-Malaysia, Armillaria root rot has been attributed to A. mellea sensu lato, although this identity almost certainly does not include A. mellea (Vahl. : Fr.) P.Kumm. sensu stricto.
Conventional identification of Armillaria has been based on the morphology of the basidiocarps, but dependence on this character is beset with problems. Generally, these structures are produced only in the final stages of the disease and then only in some years and for a limited period of time (Fox et al 1994). In some species, the morphology of the basidiocarps differs only slightly, making routine identification difficult (Bérubé and Dessureault 1989). In the past two decades, identification of unknown Armillaria isolates has depended strongly on the use of sexual-compatibility tests with known haploid tester strains (Korhonen 1978, Ullrich and Anderson 1978). However, these tests are time consuming and often yield ambiguous results. Furthermore, field isolates are usually diploid, making their sexual interaction with haploid tester strains difficult to interpret (Guillaumin et al 1991).
Problems surrounding the identification of Armillaria have led to important advances in developing robust but rapid DNA techniques. Such techniques have included DNA-base composition (Jahnke et al 1987), DNA-DNA hybridization (Miller et al 1994), sequence analyses of the first intergenic spacer region (IGS-1) (Anderson and Stasovski 1992) and internal transcribed spacer regions (ITS) (Coetzee et al 2001a), restriction-fragment length polymorphisms (RFLPs) without PCR (Smith and Anderson 1989) and RFLPs of IGS-1 amplicons (Harrington and Wingfield 1995). Although several of these techniques might include some problems (Pérez-Sierra et al 2000), by virtue of their relative simplicity they are gradually replacing traditional methods.
Sequence data for various Armillaria species have increased substantially since the first publication on the phylogeny of Armillaria in the Northern Hemisphere (Anderson and Stasovski 1992). Understandably, the initial focus of such studies has concentrated on species in Europe and North America (Chillali et al 1998, Coetzee et al 2000b). More recently, however, substantial data sets for species in Africa, Australasia and Southeast Asia have become available (Terashima et al 1998, Coetzee et al 2000a, 2001a). At present, ITS and IGS-1 sequences are available at GenBank for the best-known species of Armillaria. However, there are disjunctions in data sets and relatively little is known about species from Indo-Malaysia and South America.
The aim of this study was to identify a collection of isolates from dying trees, showing typical symptoms of Armillaria root rot in various parts of South America and Indo-Malaysia. These isolates had cultural characteristics typical of Armillaria but could not be identified based on morphology, due to the absence of basidiocarps in disease centers. In addition, isolates from a culture collection, of uncertain identity but thought to represent A. novae-zelandiae and A. limonea from Chile and Argentina, were included. Sequences from the IGS-1 and ITS regions of the rDNA operon were used to identify the unknown isolates and to determine their phylogenetic placement relative to other Armillaria species. Evolutionary relationships between field isolates from Asia and South America and isolates representing the species that shared a high ITS sequence similarity with them, were determined in a phylogenetic study using distance and parsimony analyses.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) was added to approximately 0.5 g of the powdered mycelium, vortexed and incubated for 2 h at 60 C. Cell debris was precipitated by centrifugation (15 300 g, 15 min), followed by isoamyl alcohol:chloroform (1:24) extractions on the aqueous phase (0.5 v/v) until a clean interphase was obtained. A final chloroform (0.5 v/v) extraction was done to remove the remaining isoamyl alcohol. Nucleic acids were precipitated with ethanol (100%) overnight at -20 C. The precipitate was collected by centrifugation (13 500 g, 30 min, room temperature), washed twice with ice-cold ethanol (70%), dried and dissolved in sterile distilled water. RNase A (0.01 mg/µL) was added to the suspension and incubated at 37 C for 6 h to remove contaminating RNA.
PCR and sequencing –
Extracted DNA was used as template in the PCR reactions to amplify the ITS (including ITS1, 5.8S and ITS2 regions) and the IGS-1 regions for the unknown isolates from Asia and South America. The ITS region was amplified with primer set ITS1 and ITS4 (White et al 1990) and the IGS-1 region with P-1 (Hsiau 1996) and O-1 (Duchesne and Anderson 1990). PCR reaction mixtures for amplification of the regions were the same. The mixture included dNTPs (0.25 mM of each), buffer with MgCl2 supplied by the manufacturer, additional MgCl2 (0.25 mM), 0.1 µM of each primer, ExpandTM High Fidelity PCR System enzyme mix (1.75 U) (Roche Diagnostics) and approximately 80 ng of template DNA. Reaction conditions were an initial denaturation at 96 C (2 min), 35 cycles of primer annealing at 62 C (30 s), elongation at 72 C (1 min) and denaturation at 94 C (30 s). A final elongation step was allowed at 72 C for 5 min. PCR products were purified before sequencing with a QIAquick PCR Purification Kit (QIAGEN).
Sequences for both strands of the PCR products were obtained with an ABI PRISMTM 377 automated DNA sequencer. Sequence reactions were carried out with an ABI PRISMTM Dye Terminator Cycle Sequencing Ready Reaction Kit with AmpliTaq® DNA polymerase FS (Perkin Elmer). The ITS region was sequenced with primers ITS1, ITS4, CS2B and CS3B (Coetzee et al 2001a). IGS-1 sequences were obtained with primers P-1, O-1, MCO-2 and MCO-2R (Coetzee et al 2000b).
Identification of unknown isolates –
Initial identification of the unknown isolates from Asia and South America was based on nucleotide similarity with sequences at GenBank, by using the BLAST search function of the database. In addition, ITS and IGS-1 DNA sequences for the unknown isolates were aligned with those from the same DNA regions, for the species that showed highest similarities to them. Sequence alignment was done with Clustal X version 1.8 software (Thompson et al 1997). Regions poorly aligned due to indels were manually corrected with a text editor. Aligned ITS and IGS-1 sequences for the Armillaria isolates have been deposited in TreeBase (study accession number: S771, matrix accession numbers: M1219 and M1220). Sequence similarities among isolates were determined, based on uncorrected p distances converted to percentage similarity.
Phylogenetic analyses –
Relatedness of the unknown isolates and Armillaria species showing high sequence homology to them was determined in a phylogenetic analysis based on distances and parsimony using PAUP* version 4 (Swofford 1998). Neighbor-joining (NJ) trees (Saitou and Nei 1987) were generated with a Kimura 2-parameter substitution model (Kimura 1980) implemented in the analysis and random addition of taxa. Most-parsimonious (MP) trees were generated after a heuristic search, with starting trees obtained via stepwise addition with 100 random taxon additions, branch-swapping based on the tree-bisection-reconnection (TBR) algorithm, MulTrees effective and topological constraints not enforced. MaxTrees was set to auto-increase and zero length branches were collapsed. The effect of indels on the tree topology was tested in separate analyses by exclusion of indels, inclusion of indels but with gapmode set as missing, and inclusion of indels but with gaps treated as a fifth character (newstate). Tree-length distribution of 100 randomly generated trees was determined for phylogenetic signal (g1) (Hillis and Huelsenbeck 1992). Confidence in branching points on the phylogenetic trees was determined with bootstrap (1000 replicates) (Felsenstein 1985).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The unknown Chilean and the presumed A. limonea isolate from Argentina had ITS sequences that were most similar to ITS sequences for A. luteobubalina Watling & Kile at GenBank. ITS sequences for these isolates also were very similar to those for A. limonea in the database, but their scores were significantly lower, 737–745 in contrast to the 930–944 bits obtained for A. luteobubalina. Isolates CMW8876 and CMW8879 from Chile had identical ITS sequences but differed from isolate CMW5446 in Argentina (<1%) due to a single 32bp indel. IGS-1 sequences for isolates CMW8876, CMW8877 and CMW8879 from Chile and CMW5446 from Argentina were identical. IGS-1 sequences for these isolates showed a 95% similarity with unpublished IGS-1 sequences of A. luteobubalina (CMW4977). Armillaria limonea (CMW4991) had IGS-1 sequence similarity of 85% with the isolates from Chile and Argentina.
Phylogenetic analyses –
The choice of taxa in the ITS data set could be made only after initial identification of the unknown isolates. Thus ITS sequence data for A. limonea (CMW4678 and CMW4680), A. luteobubalina (CMW4977 and CMW5704), and A. novae-zelandiae (CMW4722 and CMW4964) (Table II) were used to determine the phylogenetic relationships among the isolates. Armillaria hinnulea Kile & Watling (CMW4983 and CMW4990) (Table II), a Southern Hemisphere species (Coetzee et al 2001a) shown to be closely related to Northern Hemisphere species, was used as the outgroup.
The presence of large indels in the data set had a minimal effect on parsimony analyses (Table III). Most-parsimonious trees generated with indels treated in different ways were similar in overall topology (Fig. 1). Swapping between taxa on the terminal branches resulted in multiple MP trees when indels were excluded or included but gaps treated as missing. The placement of the unknown taxa within specific clades, however, was supported by bootstrap values, independent of the treatment of indels.
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Isolate CMW5446 from Argentina, thought to represent A. limonea, grouped closely in a well-supported clade with the isolates from Chile (CMW8876 and CMW8879) in both NJ and MP trees generated (Fig. 1). These isolates, identified as A. luteobubalina based on ITS sequence similarity, resided in a highly supported group that included authentic isolates representing A. luteobubalina (CMW5704 and CMW4977). The South American group of isolates, however, formed a sister group to the A. luteobubalina clade in distance and parsimony analyses, with indels excluded or with indels included but gaps treated as missing.
The relationships among the unknown isolates from Chile and Argentina and those of A. luteobubalina were further investigated based on their IGS-1 sequences. The number of characters included in the data set was 537, after exclusion of an ambiguously aligned CT rich region. Trees generated on distance and parsimony analysis had similar topologies and grouped the Chilean and Argentinean isolates in a strongly supported monophyletic group (Fig. 2). Isolates representing A. luteobubalina from Australia formed a well-supported monophyletic sister group with the South America isolates. Isolates representing A. limonea from New Zealand were placed basal to the South American A. luteobubalina.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) regarding the identity of species in South America. Our results also provide interesting new records pertaining to the distribution of Armillaria species in the areas considered. Results from this study have confirmed the utility of sequence data for identifying Armillaria in the absence of basidiocarps. Moreover, they add substantial new information regarding phylogenetic relationships for this important group of root pathogens.
Two isolates from Chile, of uncertain identity but resembling A. novae-zelandiae based on basidiocarp morphology, were included in this study. Phylogenetic analyses confirmed their identity as A. novae-zelandiae by placing them in a strongly supported monophyletic group, with well-recognized isolates of this species from Australia and New Zealand. There were, however, some differences in the ITS sequences between the Chilean isolates and those from Australia, due to indels and base substitutions. Differences between Australasian and South American collections of A. novae-zelandiae have been reported by Kile and Watling (1983), and our data support their observations.
Although Armillaria has been shown to be introduced into new areas (Coetzee et al 2001b), it is unlikely that A. novae-zelandiae was introduced into Chile from Australia or New Zealand. The ITS sequences of the Australian, Chilean and New Zealand isolates, although highly similar, differed as a result of a number of indels. These differences suggest a long period of geographic separation between A. novae-zelandiae from Australasia and South America. Furthermore, isolates from Chile were collected from Nothofagus, a genus that occurs in Chile, Argentina, Australia, New Zealand, New Guinea and New Caledonia. Nothofagus species formed a continuous forest from New Guinea, through eastern Australia, west Antarctica, New Zealand-New Caledonia to southern South America when these landmasses were part of the supercontinent Gondwanaland (Poole 1987). Kile et al (1994) noted that A. novae-zelandiae in Australia displays a particularly close association with Nothofagus. Likewise Singer (1953) and Horak (1983) noted relationships among fungi on Nothofagus in Australia, New Zealand and South America. The close phylogenetic relationship between the South American, Australian and New Zealand isolates of A. novae-zelandiae supports the notion that this fungus was associated with Nothofagus before the breakup of Gondwana and that it is native to South America.
Sequence-data comparisons lead us to tentatively identify isolates from Malaysia and Indonesia as A. novae-zelandiae. However, distance and parsimony analyses revealed that they form a strongly supported monophyletic group basal to the South American-Australia-New Zealand clade representing this species. Although these isolates are closely related to A. novae-zelandiae, it is possible that they represent a discrete taxon. This could be a species already known but for which sequence data are not available, or alternatively, it could represent an undescribed taxon.
At least eight species of Armillaria have been reported in Japan, and many of these are known or related, based on IGS-1 sequences, to those in other parts of the Northern Hemisphere (Terashima et al 1998). Although IGS-1 sequence data were not obtained for the Malaysian and Indonesian isolates in this study, it previously had been shown that the Southern Hemisphere Armillaria species differ significantly in their ITS sequences from those in the Northern Hemisphere (Coetzee et al 2001a). It also was shown that A. hinnulea (used as outgroup in this study) is more closely related to the Northern Hemisphere species than to the species in the Southern Hemisphere (Coetzee et al 2001a). Thus the placement of the isolates from Indonesia and Malaysia within a strongly supported monophyletic clade, including the exclusively Southern Hemisphere A. novae-zelandiae and distant to A. hinnulea, makes it unlikely that the isolates in Malaysia and Indonesia represent one of the known Japanese species.
It is unlikely that isolates from Indonesia and Malaysia in this study are related to species in India, despite the fact that India formed part of Gondwana. This view is supported by the findings of Kile and Watling (1988) who showed, based on morphology, that Indian species of Armillaria are most closely related to Northern Hemisphere species. Similarly Volk and Burdsall (1995) showed that Australian and New Zealand Armillaria species do not occur in India. The close phylogenetic relationship among isolates from Indonesia and Malaysia and A. novae-zelandiae from Australia and New Zealand, and the previously reported morphological differences between Australian and Indian Armillaria species, reduces the likelihood that the Indonesian and Malaysian isolates in this study represent one of the Indian species.
A surprising discovery in this study was the fact that some isolates from Chile and one from Argentina were found to represent A. luteobubalina. This species has previously been known only in Australia, where it is a well-known pathogen of Eucalyptus (Kile et al 1991, Volk and Burdsall 1995). The isolate from Argentina originated from a basidiocarp resembling A. limonea on Nothofagus antarctica. Armillaria limonea first was described in New Zealand as Armillariella limonea G.Stev. (Stevenson 1964) but also was found in a Nothofagus forest in South America by Singer (Singer 1969). The ITS sequence of the suspected A. limonea isolate was highly similar to the isolates from an exotic Pinus radiata plantation in Southern Chile and for which basidiocarps were not found. Although we expected the unknown Chilean isolates to represent A. limonea, their ITS sequences and that of the Argentinean isolate are closest to A. luteobubalina. Phylogenetic analyses, based on parsimony and distances, further supported the results based on sequence similarity, by placing the South American isolates within a strongly supported monophyletic group with A. luteobubalina. The Argentinean and Chilean isolates, however, were separated from the Australian group by large indels.
The unexpected grouping of Chilean and Argentinean isolates with A. luteobubalina justified our further analysis based on sequences of the IGS-1 region. DNA sequences for this region previously have not been determined for any of the Australian and New Zealand species. Results unequivocally confirmed findings based on ITS sequences, that isolates from Argentina and Chile represent A. luteobubalina, forming a strongly supported monophyletic group with this species.
Although from different countries, the Chilean and Argentinean isolates of A. luteobubalina probably originated from areas relatively close to each other. The Chilean isolates were collected from dying P. radiata in the lower Andes and certainly originated in native vegetation, which predominantly includes Nothofagus. In Argentina, Nothofagus occurs in the Andes and the origin of the Argentinean isolate from this tree suggests a proximity of origin. The presence of A. luteobubalina in South America also suggests that this species has an early Gondwanan origin. This is the best-known species of Armillaria in Australia, where it occurs transcontinentally in natural wet and dry sclerophyll eucalypt forests as well as in horticultural plantings (Kile and Watling 1981, Shearer 1994). The wide distribution of this species in Australia, as well as its discovery in South America, support the view that it is an ancient species, with an origin preceding the separation of Gondwana. The fact that the South American isolates were separated from the Australian group in both ITS and IGS-1 trees, supports an extended period of geographical separation. Although available data support treating them as a single species, isolates clearly have existed independently for a long period and later might be regarded as independent taxa.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Accepted for publication August 31, 2002.
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LITERATURE CITED |
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