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Forestry and Forest Products Research Institute, Tsukuba, Ibaraki 305-8687, Japan
Sawako Tokuda
Hokkaido Forestry Research Institute Koshunai, Bibai, Hokkaido 079-0198, Japan
Peter K. Buchanan
Landcare Research, Private Bag 92170, Auckland, New Zealand
Tsutomu Hattori
Forestry and Forest Products Research Institute, Tsukuba, Ibaraki 305-8687, Japan
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The phylogenetic relationships of two Japanese Heterobasidion species, H. annosum sensu lato and an undetermined species, were revealed based on three gene loci, glyceraldehyde 3-phosphate dehydrogenase (gpd), heat shock protein (hsp) and elongation factor 1-
(ef). The tree, based on combined data of gpd, hsp and ef, showed that Japanese H. annosum s.l. was close to the European S-group, forming a subclade. The results of this study also provided strong support for the recognition of the undetermined Heterobasidion sp. as a distinct phylogenetic species closely related to H. araucariae.
Key words: elongation factor 1-, glyceraldehyde 3-phosphate dehydrogenase, heat shock protein, polypore, taxonomy
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Heterobasidion annosum (Fr.) Bref. sensu lato is widely distributed in the northern hemisphere from central Finland in the north to northern Africa and Central America in the south (Korhonen et al 1998). It consists of five closely related groups that are more or less intersterile. They are classified based on their host preferences and distribution: (i) European pine group (Eur P-group), (ii) North American pine group (NAm P-group), (iii) European spruce group (Eur S-group), (iv) European fir group (Eur F-group) and (v) North American spruce group (NAm S-group). The European members of the H. annosum complex were named by Niemelä and Korhonen (1998) as H. parviporum Niemelä & Korhonen (=Eur S-group), H. abietinum Niemelä & Korhonen (=Eur F-group) and H. annosum sensu stricto (Eur P-group). The Eur P-group shows preference for Pinus sylvestris L. (Korhonen and Stenlid 1998) and causes death in P. sylvestris stands of all ages (Bendz-Hellgren et al 1998). However it attacks many other conifers and broadleaf trees as well. The NAm P-group is also an important pathogen in pine stands of the western and southeastern USA. The Eur S-group shows relatively strict specialization for Picea abies (L.) Karst. and occurs primarily in areas where P. abies grows naturally. Only P. abies seedlings and young trees normally are killed by Eur S-group in the Nordic countries (Bendz-Hellgren et al 1998). Eur F-group shows preferences for Abies alba Mill. although it can infect other hosts as well and it occurs where Abies species grow naturally in southern and central Europe. In some contrast with the Eur S- and F-groups, the NAm S-group does not show a high degree of host specialization (Korhonen et al 1998).
In addition to H. annosum s.l. other species of Heterobasidion are known from eastern Asia and Australasia. Heterobasidion araucariae P.K. Buchanan is the only species reported from Australasia, where it inhabits dead conifer wood (Buchanan 1988). Heterobasidion insulare (Murrill) Ryvarden is distributed mainly in eastern Asia and is reported to be a saprobe. Heterobasidion insulare was found to comprise a species complex based on mating tests and DNA analyses (Dai et al 2002).
In Japan two Heterobasidion species, H. annosum s.l. and H. insulare, have been reported (Ito 1955, Núñez and Ryvarden 2001). The distribution of H. annosum s.l. in Japan is restricted to the subalpine zone in Hokkaido and in central Honshu (Ito 1955, Ono and Yokota 1959). The main host species are Abies sachalinensis (Schmidt) Mast. and Picea glehnii (Schmidt) Mast. in Hokkaido (Kamei and Hoshi 1948, Yokota 1956) and on Abies mariesii Mast. and A. veitchii Lindl. in central Honshu (Aoshima 1952). Japanese H. annosum s.l. is considered to be a decay fungus occasionally causing root and butt rot on conifers (Ito 1955, Ono and Yokota 1959), while H. insulare is widely distributed from Hokkaido to Kyushu. It is a saprobe of coniferous trees in Japan (Ito 1955, Núñez and Ryvarden 2001). In addition an undetermined Heterobasidion species has been recorded from warm temperate areas of the main islands and in subtropical areas of the southern islands of Japan. This undetermined species is macromorphologically distinguishable from the known Heterobasidion species by absence of a dark crust at the pileus surface.
Analyses based on the sequences of the internal transcribed spacer region (ITS) and the intergenic spacer region (IGS) of the nuclear rDNA (Harrington et al 1998) peroxidase genes (Maijala et al 2003) and laccase genes (Asiegbu et al 2004) showed the outline of the phylogeny of Heterobasidion spp. Heterobasidion araucariae and H. insulare were shown to be distinct from H. annosum sensu lato (Asiegbu et al 2004, Maijala et al 2003, Harrington et al 1998). In the groups of H. annosum s.l., the analyses based on ITS and IGS region by Harrington et al (1998) delimited three major lineages within H. annosum s.l., Eur-P clade (as H. annosum sensu stricto), NAm-P clade and the ‘‘fir form’’, including isolates of NAm S-group and Eur S/F-group. Asian isolates including three Japanese isolates formed a weakly supported subclade in the ‘‘fir clade’’. Manganese peroxidase amino acid sequences (Maijala et al 2003) indicated weak separation of the European, Asian and American isolates of H. annosum s.l. Based on isozyme and RAPD analyses, Eur S- F-, and NAm S-groups are reported to be genetically isolated (Garbelotto et al 1998, Karlsson and Stenlid 1991, La Porta et al 1997, Otrosina et al 1993). The analyses based on five gene fragment sequences by (Johannesson and Stenlid 2003) separated H. parviporum (Eur S-), H. abietinum (Eur F-) and NAm S-groups into three clades, and Japanese strains of H. annosum s.l. were shown to be closely related to H. parviporum. Few Japanese isolates were examined in the above studies, and most were isolated from decayed wood without basidiocarps.
This study seeks to clarify the phylogenetic placement of Japanese H. annosum s.l. and the undetermined Heterobasidion sp. within the genus Heterobasidion using Japanese isolates derived from basidiocarps. The fragments of three nuclear genes reported by Johannesson and Stenlid (2003) were used for the analyses.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Mycelia for DNA extraction were grown 1 wk on liquid MYG medium (2% [w/v] malt extract, 0.2% [w/v] yeast extract, 2% [w/v] glucose) at 25 C in the dark. DNA was extracted with a DNeasy plant minikit (QIAGEN). The fragments of three nuclear genes, elongation factor 1- (ef), glyceraldehyde 3-phosphate dehydrogenase (gpd) and heat shock protein (hsp) were used as molecular markers. Oligonucleotide primers used in this study were reported in Johannesson and Stenlid (2003). The ef fragment of H. araucariae and Heterobasidion sp. did not successfully amplify with EF1f and EF1r of Johannesson and Stenlid (2003). Additional primers (EF1-526F and EF1-1567R, http://ocid.nacse.org/research/deephyphae/EF1primer.pdf) were used. Each PCR contained approximately 10 ng of template DNA, 10 mM Tris -HCl (pH 8.3), 50 mM KCl, 1.5 mM MgCl2, 0.2 µM of each primer, 2.5 mM of each dNTP, and Takara taq (0.5 U) (Takara) in a total volume of 20 µL. PCR amplification was performed with a Perkin-Elmer DNA thermal cycler (9800) or BIO-RAD iCycler. PCR conditions for ef, gpd and hsp of Heterobasidion isolates included 5 min at 94 C, followed by 35 cycles of 1 min at 94 C, 30 s at 50–56 C, and 30 s at 72 C, with a final extension of 7 min at 72 C. In addition these programs were used to amplify ef fragments with primers EF1-526F and EF1-1567R: 5 min at 94 C, followed by 10 cycles of 1 min at 94 C, 30 s at 60–50 C and 30 s at 72 C (temperature decreased 1 C for each of the 10 cycles), followed by a remaining 30 cycles, with a final extension of 7 min at 72 C. PCR products were purified either directly with MicroSpin Columns and Sephacryl S-300 (Amersham Biotech) or following agarose gel electrophoresis and band excision with Mono Fas DNA Kit I (GL Science). Some PCR products of hsp gene fragments were cloned into the pGEM-easy vector (Promega) and at least eight clones from each isolate were sequenced. All sequences were determined in both directions with BigDye Terminator cycle sequencing FS Ready Reaction Kit with an Applied Biosystems 3100 sequencer (Perkin-Elmer).
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). Sequence data for European and American strains were derived from GenBank (TABLE II). Sequences were aligned with Clustal x (Jeanmougin et al 1998) and adjusted manually. The sequence alignments have been deposited in TreeBASE as submission No. SN2197. Only unambiguous alignments were used in phylogenetic analyses. Echinodontium tsugicola (Henn. & Shirai) Imazeki, which was one of the close relatives of Heterobasidion spp. (Binder and Hibbett 2002), was used as outgroup in the phylogenetic analyses. Phylogenetic analyses of the aligned sequences were performed with distance, parsimony and likelihood methods in PAUP version 4.0b10 (Swofford 2001). For distance analyses, neighbor joining (NJ) generated from HKY 85 distances was performed. Maximum parsimony (MP) trees were generated by heuristic searches with random stepwise addition of sequences (100 replicates), TBR (tree bisection reconnection) branch swapping and MULTREES effective. MAXTREES initially was set to 1000 and zero length branches were collapsed. All characters were of equal weight and unordered. The gap-mode was set as NEWSTATE. The strength of the internal branches of the resulting trees was statistically tested by bootstrap analysis (Felsenstein 1985) from 1000 bootstrap replications. Clades with bootstrap values >70% were considered strongly supported by the data. To determine which model of nucleotide substitution with the least number of parameters best fit each dataset, hierarchical likelihood ratio tests were performed as implemented in the program Modeltest version 3.7 (Posada and Crandall 1998, Posada 2005). Estimated model parameter values resulting from the Modeltest run were entered into PAUP, and maximum likelihood (ML) analyses consisting of heuristic searches with TBR branch swapping were performed. Before combined analyses partition homogeneity test was performed to determine whether three datasets could be combined into a single analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). All loci possessed both intron and protein-coding regions. A few polymorphic positions also were in the coding regions of ef and gpd loci but no amino-acid change was shown. The best-fit model selected for likelihood by Modeltest was GTR+G model for gpd and hsp, and K80(K2P)+G model for ef. NJ, MP and ML trees based on each region were similar in overall topology. Outgroup sequences are divergent from those of the ingroup. Rooting with outgroups and midpoint rooting were tested for their effect on both the ingroup topology and placement of the root (Sanderson and Shaffer 2002). Because all gave similar results trees using midpoint rooting are shown in this study.
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): Eur F-group (>95% of bootstrap value), NAm S-group (>74%), Eur and NAm P-group (>75%), Heterobasidion sp. (>95%), and H. araucariae (>95%). Heterobasidion insulare formed a strongly supported clade in the gpd (93%) and ef (100%) trees but a comparatively weakly supported clade in the hsp tree (66%). Eur S-group and Japanese H. annosum s.l. were grouped together and formed a strongly supported clade in gpd (96%) and hsp trees (95%). However in the ef tree Eur S-group and Japanese H. annosum s.l. were separated, with Eur S-group forming a weakly supported clade (66%) and Japanese H. annosum s.l. forming a strongly supported clade (92%). In hsp and ef trees (FIG. 1b, c), the isolates of Heterobasidion sp. formed a strongly supported sister clade (>96%) with H. araucariae. The partition homogeneity test was not significant between gpd and hsp, and between gpd and ef (P = 0.07 and 0.08, respectively). However comparison among hsp and ef and three genes produced a significant partition homogeneity test (P < 0.01). The strict consensus tree based on gpd and hsp was similar to that of the three-gene combined data, except that the three-gene tree indicated monophyly of each S-group and Japanese H. annosum s.l. with high bootstrap value (data not shown). The homogeneity partition tests using the data of. H. annosum s.l. (Eur S, NAm S, Japanese H. annosum s l., Eur F, Eur P and NAm P isolates) showed no conflict for any of the pairs of three-gene loci (P > 0.01) and the tree topology was congruent with the tree based on three gene loci using all isolates. Therefore in this study gpd, hsp and ef data were combined into a single analysis. A single MP tree produced from analysis of the combined dataset of gpd, hsp and ef (FIG. 1d) showed that each of Eur S-, Japanese H. annosum s.l., NAm S-, Eur F-, H. insulare, Heterobasidion sp., H. araucariae and Eur and NAm P-groups formed a strongly supported clade. Japanese H. annosum s.l. isolates were grouped together with Eur S-group clade (100%). Eur S-, Japanese H. annosum s.l. and NAm S-group were grouped together with the Eur F-group as the sister clade (83%). Heterobasidion sp. isolates were grouped together with the H. araucariae clade (100%). Eur- and NAm P-groups are closely related to H. insulare, Heterobasidion sp. and H. araucariae, forming a monophyletic group.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The S-lineage is thought to have migrated to Europe from eastern Asia with its host species (Korhonen et al 1997, Johannesson and Stenlid 2003). In addition Eur S-group should have a more recent genetic bottleneck by the implications of glaciations, compared to Japanese populations, because present-day Picea abies spread from some limited refuges after the ice age (Vidakovi
1991). Of interest, some isolates from Urals and northeastern China were included in ‘‘Eur S-clade’’ in this result. More Asian isolates should be included in analyses to clarify the relationship between Eurasian and Japanese populations.
The high level of pathogenicity shown by Eur S-group on Picea abies and A. sibrica in Europe and western Siberia appears to decline in eastern Asia (Dai et al 2003). Japanese H. annosum s.l. is distributed mainly in old growth natural forests in Hokkaido and in the alpine zone in Honshu Island. There are no records of this fungus occurring primarily in young plantations in Japan. Root rot caused by Japanese H. annosum s.l. recently was found in a plantation of 68 y old A. sachalinensis in Hokkaido (Tokuda et al 2007). In their study the growth rings of decayed trees were as well developed as those of healthy trees and there was no symptom of tree decline in and around the study site. Japanese H. annosum s.l. is considered to have low pathogenicity to Japanese hosts compared with the pathogenicity of Eur S-group to European host trees.
Eur F- and NAm S-groups formed strongly supported distinct clades in each of the three gene fragment trees and the combined data tree. In the combined data tree NAm S-group formed a sister clade with Eur S-group/Japanese H. annosum s.l. and Eur F-group is basal to these three groups. The phylogeny of Abies spp. based on chloroplast DNA sequences (Suyama et al 2000) showed three main lineages: (i) Asian group (including two North American species), (ii) North American (including A mariesii) and (iii) European clades. The phylogenetic relationship of Picea spp. unfortunately has not been resolved because of the close relationships among species. The distribution of NAm S-group overlaps the distribution of western North American Abies spp. (Korhonen and Stenlid 1998). Japanese H. annosum s.l., NAm S-group and Eur F-group appear to be related to the evolutionary history of Abies spp.
This study showed that an undetermined Japanese Heterobasidion sp. is closely related to H. araucariae but formed a well differentiated genetic lineage within the genus Heterobasidion. Heterobasidion insulare formed a group along with H. araucariae and Japanese Heterobasidion sp. Basidiocarps of the Japanese Heterobasidion sp. differ morphologically from H. araucariae and H. insulare in the lack of a distinct crust or with the crust restricted to the basal area of the pileus. Heterobasidion araucariae has a brown to red-brown or dark brown crust on the pileus surface except at the margin (Buchanan 1988) and H. insulare has a dark and distinct cuticle on the pileus surface of mature basidiomata (Núñez and Ryvarden 2001).
Japanese Heterobasidion sp. usually is seen fruiting on dead standing trees or cut stumps of Pinus luchuensis Mayr. in the southern islands of Japan and on P. densiflora Sieb. et. Zucc. in the warm temperate region of the Japanese main islands. Heterobasidion araucariae has a restricted host range: two species of Agathis Salisb., two species of Araucaria Juss. and three species of Pinus L. in eastern Australia, New Zealand, Papua New Guinea and Fiji (Buchanan 1988). Heterobasidion insulare occurs on dead wood of Abies, Pinus and Picea in southern and eastern Asia: Himalaya, Burma, Philippines, China, eastern Russian and Japan (Niemelä and Korhonen 1998). In southeastern Asia, Corner (1989) reported H. annosum on Agathis and Podocarpus L’Herit. from the mountains of Borneo. His description suggests that this might represent H. araucariae with a thick corky context and a brown crust. Heterobasidion arbitrarium (Corner) T. Hatt., also reported from the mountains of Borneo, has a thick and corky context without a crust (Hattori 2003). The relationships among these species and H. araucariae, H. insulare and Heterobasidion sp. have not been investigated.
From results of the combined data in this study, the clade consisting of Eur P- and NAm P- isolates grouped together with H. insulare, H. araucariae and Heterobasidion sp. Data from only one isolate of each of Eur P- and NAm P-groups were used in this study, limiting discussion of relationships among these groups and the phylogenetic position of the P-groups. However our results are congruent with related studies using sequences of ITS and IGS regions of nrDNA, in which Eur P- and NAm P-groups are similar and are more closely related to H. insulare and H. araucariae than to the S- and F-groups (Harrington et al 1998, Michelson and Korhonen 1998). In analyses based on the IGS region the Eur P-group grouped more closely with H. insulare than with NAm P-group (Harrington et al 1998). Harrington et al (1998) mentioned that where no pine form of H. annosum is known (i.e. Asia) H. insulare appears to be common, although it occupies a different ecological niche. Allopatric speciation of H. insulare and P-groups could explain this observation.
Further knowledge of Asian species of Heterobasidion is relevant to understanding the evolutionary history of Heterobasidion and species concepts within the genus. Additional studies including Asian populations are necessary to clarify the taxonomy, phylogeny and evolution of the genus Heterobasidion.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: yuota{at}ffpri.affrc.go.jp
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LITERATURE CITED |
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