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Department of Applied Chemistry and Microbiology, P.O. Box 56, 00014 University of Helsinki, Finland
Thomas C. Harrington 1
Department of Plant Pathology, 351 Bessey Hall, Iowa State University, Ames, Iowa 50011, USA
Marjatta Raudaskoski
Department of Biosciences, Division of Plant Physiology, P.O. Box 56, 00014 University of Helsinki, Finland
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Four putative peroxidase-encoding gene fragments, named mnp1a, mnp1b, mnp2 and mnp3, were amplified with degenerative primers from the white-rot basidiomycete genus Heterobasidion. The fragments were cloned and sequenced. Similar fragments were produced and analyzed from the related genera Amylostereum, Bondarzewia and Echinodontium. Each amplified fragment contains three identically positioned introns. According to the predicted amino acid sequence, these fragments are most similar to two Mn peroxidase-encoding genes (MPGI and mnp2) and gene pgv of Trametes versicolor. Conserved residues thought to be essential for peroxidase function were identified. All four MnP gene loci of Heterobasidion were detected only in H. parviporum. Variation occurred in the predicted amino-acid sequences (131–132 amino acids) of all four fragments originating from the 47 Heterobasidion isolates tested. Amino acid variation in fragments of mnp2 and mnp3 separated European Heterobasidion parviporum ("S-type") and H. abietinum ("F-type"), known to have identical rDNA sequences. Asian and western North American isolates from fir, spruce and other hosts had the peroxidase amino acid sequences of European H. parviporum. American and European H. annosum ("P-type") isolates had different amino acid sequences and might be cryptic species.
Key words: Amylostereum, Bondarzewia, Echinodontium, manganese peroxidase, phylogeny
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In general, H. parviporum (=H. annosum S group) is a specialized pathogen of Norway spruce, Picea abies; H. abietinum (=H. annosum F group) infects firs (Abies spp.); and H. annosum (=H. annosum P group) occurs primarily on pines (Pinus spp.). Groupings are based primarily on interfertility as determined by clamp formation (Korhonen 1978, Capretti et al 1990), but the groups also show differences in physiological and biochemical characteristics (Karlsson and Stenlid 1991, Otrosina et al 1993). The relationships of H. annosum populations from Asia and North America to those in Europe are not clear (Harrington et al 1998).
Heterobasidion species are able to degrade lignin, and H. annosum is known to secrete laccase (Haars et al 1981, Haars and Hüttermann 1983), but peroxidase activity has been difficult to demonstrate in pure cultures (Haars et al 1981, Boudet et al 1988). In the basidiomycete white-rot fungi, lignin peroxidases (LiPs) and manganese peroxidases (MnPs) are involved in the biodegradation of lignin, and MnP seems to be present in almost all white-rot fungi (Hatakka 1994). Flecks of MnO2 in wood decayed by H. annosum (Blanchette 1984) suggest the presence of MnP activity, and three MnP isozymes have been identified from a homokaryotic isolate of the European H. annosum when the fungus was cultivated on spruce wood chips (Maijala 2000).
Knowledge of the molecular genetics of lignin-degrading enzymes has proceeded rapidly during the past decade, especially in the basidiomycete Phanerochaete chrysosporium (Cullen 1997, Gold and Alic 1993). More than 50 different fungal peroxidase gene sequences are available from 12 different basidiomycete species, which allows comparative studies of the peroxidase gene structure and evolution.
Using degenerative PCR primers designed from previously identified MnPs, Maijala et al (1998a, b) we amplified and cloned a partial sequence of a putative MnP gene from H. annosum. Here we report the structure and variation of the amino acid sequences of four putative MnP gene fragments in H. parviporum, H. abietinum, H. annosum, H. araucariae and H. insulare, and similar fragments in the closely related genera Amylostereum, Bondarzewia, and Echinodontium. The peroxidase gene sequences have been used to re-evaluate the phylogeny of Heterobasidion.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. Most of the Heterobasidion isolates were confirmed to be H. abietinum, H. annosum or H. parviporum, based on dikaryon formation with tester strains. The collection information on Amylostereum and Echinodontium species can be found in Tabata et al (2000).
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. Degenerative forward and reverse PCR primers were designed from multiple fungal peroxidase sequence alignments, revealing consensus areas in the putative Ca2+-binding motifs in the enzyme (Poulos et al 1993). The respective forward and reverse primers were DP1 (5'-GG(A/C/T)GGTGCCGATGG(C/G)TC-3') and DP2 (5'-GG(A/G)GTGGAGTC(A/G)AACGG-3'). More specific primers used for each of the three peroxidases in Heterobasidion were PX11 (mnp1-specific, forward, 5'-GATGGGTCCATCATCGTA-3'), PX12 (mnp1-specific, reverse, 5'-GAGTTCCTGGGATCGTCAC-3'), PX21 (mnp2-specific, forward, 5'-TGCCGATGGGTC(A/G/T)ATATC-3'), and PX31 (mnp3-specific, forward 5'-GATGGGTCCCT(C/T)AT(C/T)GTG-3'). These primers amplify a fragment of about 570 bp. In general, PCR included 50 pmol of each primer, 50–100 ng of genomic DNA, 2 mM dNTPs, 1.5 mM MgCl2, and 2.5 units of DNA-polymerase (Promega) per 100 µL reaction. Cycling conditions typically included an initial denaturation at 94 C for 95 s and 34 cycles of 94 C for 35 s, 52 C for 1 min, and 72 C for 2 min, with a final elongation of 10 min at 72 C. Slow ramping (1 C for every 5 s) was used from annealing to extension temperatures. Resulting products were cut from the agarose gel and cloned into the pGEM-easy vector (Promega). For sequencing, cloned products were cycle-sequenced with an automated ABI sequencer in both directions with the T7 and SP6 universal primers that flank the cloning site.
Representative DNA sequences and inferred amino-acid sequences of the amplified fragments were deposited in GenBank (AJ507469–AJ507485). The mnpA fragments from Amylostereum and Echinodontium species were deposited in GenBank with accession numbers AF218404 (A. areolatum), AF218405 (A. ferreum), AF218408 (A. laevigatum), AF218410 (E. tinctorium), and B. montana peroxidase fragments by AF218413 and AF218414 (Tabata et al 2000). Other available amino acid sequences were downloaded from various sources: Trametes versicolor pgv = X77154, mnp2 = AF102515, mpg1 = Z30668, vlg2 = M91818, lpgIII = Z30666, vlg1 = M55294, lpgIV = Z31011, lpgII = Z75655, npr = AF008585; Phlebia radiata lgp3 = 126290; Phanerochaete chrysosporium lipB = X54257, lipG = AF140063, lipI = O282 (Schalch et al 1989), lipE = L08963, lipA = M27884, lipC = X55343, lipF = M77508, lipH = M24082, lipJ = AF140062, lipD = M18743; Bjerkandera adusta lpo1 = 444058; Trametes hirsuta lip = E07702; Ceriporiopsis subvermispora mnp1 = AF013257, mnp3 = AF161585, mnp2a = AF161078, mnp2b = AF161584; fungus IZU-154, (Matsubara et al 1996); Dichomitus squalens mnp1 = 157474, mnp2 = 157475; Pleurotus ostreatus mnp1 = U21878, mnp2 = AJ243977; Pleurotus eryngii mnpl = AF007224; and Coprinus cinereus cip1 = X70789.
Putative amino-acid sequences were analyzed with parsimony (PAUP 4.0b3a, Swofford 1998) after manually aligning the sequences by inserting gaps. A total of 136 characters, including gaps, were in the aligned data set. Gaps were treated as missing data. Maximum-parsimony heuristic searches were performed with all characters having equal weight and with tree-bisection-reconnection. The robustness of the internal branches of the tree was evaluated by 100 bootstrap replications using heuristic searches.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and peroxidase-encoding genes in Pleurotus species share the three intron positions with the fragments investigated but have additional intron(s) within the analyzed region (Fig. 1). All peroxidase fragments of Heterobasidion, as well as the peroxidase fragments of B. montana, Amylostereum, and Echinodontium species, possess the predicted consensus splice sites GT(a/g)NG(c/t) for the 5' end and (c/t)N(c/t)AG for the 3' ends of eukaryotic introns (Ballance 1986).
In all Heterobasidion, Amylostereum, Bondarzewia and Echinodondium fragments, the position of intron I matches exactly the position of the third intron in T. versicolor MnP encoding gene MPGI (Johansson and Nyman 1996) and LiP encoding genes LPG1, LPGIII, LPGIV (Jönsson and Nyman 1994, Johansson and Nyman 1996) and VLG1 (Black and Reddy 1991). This intron position also is shared with Pleurotus ostreatus mnp-genes (Asada et al 1995, unpubl) and with P. eryngii versatile peroxidase encoding gene mnpl (Ruiz-Dueñas et al 1999). The positions of introns II and III match those in all P. chrysosporium LiP genes (Gold and Alic 1993) and mnp-genes of the Pleurotus species. MnP genes from Ceriporiopsis subvermispora (Lobos et al 1998, Tello et al 2000), Dichomitus squalens (Li et al 1999) and P. chrysosporium have no intron positions in common with Heterobasidion (Fig. 1).
Structural and functional domains –
The amplified region includes several structural and functional domains that are conserved in all fungal secretory peroxidases (Table III), such as the invariant proximal His177 ligand to the heme (based on T. versicolor MPGI-gene numbering; Johansson and Nyman 1996) and calcium-binding regions including residues Gly67, Asp69, Ser71, Thr/Ser178, Asp195, and Thr197 (Sundaramoorthy et al 1994). In the three-dimensional structure of LiP and MnP, residues Phe82, His83, Pro/Ala84, and Asn85 are located at the surface of the protein, and they form one putative, long-range electron transfer (LRET) pathway (Schoemaker et al 1994, Camarero et al 1999). In mnp3 and mnpA, position 82 is occupied by a redox-active Tyr-residue, so far only found in one of the P. chrysosporium LiP H2 isozyme-encoding genes, lipD (de Boer et al 1987) and in a manganese-repressible peroxidase of T. versicolor (Collins et al 1999). The presence of two glycine residues at the site that represents the heme-opening channel in the three-dimensional structure (Poulos et al 1993, Sundaramoorthy et al 1994) is another distinct feature of the mnp3 fragments of different Heterobasidion species and A. areolatum mnpC. Cysteine residues in fungal secretory peroxidases are all conserved, and the cysteine occupying Position 121 is invariant in the analyzed fragments, except in one H. parviporum fragment (Fig. 2). An atypical Cys is found in A. areolatum mnpC at Position 109 and in B. montana mnpB at position 132.
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). Asp183 residue is present in all the cloned and sequenced fragments, except in the mnpB fragment from B. montana, in which Asp183 is replaced by a glutamine. In the other MnP-fragment from B. montana (mnp2), the correct Asp183 residue needed for Mn2+ binding is present. Potential N-glycosylation sites (Asn-X-Thr/Ser) (Kornfeld and Kornfeld 1985) are not markedly conserved among the genes or species analyzed in this study (Fig. 2).
Phylogenetic analyses of putative amino acid sequences –
Examination of the aligned amino acid sequences (Fig. 2) suggests that the fragments amplified from Heterobasidion, Bondarzewia, Amylostereum and Echinodontium are similar and distinct from those of the amino-acid sequences of peroxidases identified in other white-rot fungi. In the results of the parsimony analysis shown in Fig. 3, the tree is rooted to Coprinus cinereus peroxidase, which belongs to a separate class of secretory fungal peroxidases (Baunsgaard et al 1993). There is no bootstrap support for the branch containing the representative sequences of the fragments of Heterobasidion, Bondarzewia, Amylostereum and Echinodontium, but this clade was inferred in all six most-parsimonious trees. The amino acid sequences of T. versicolor MnP encoding genes mnp2 (unpubl), MPGI (Johansson and Nyman 1996) and a gene pgv (Jönsson et al 1994) appear to be most similar to those of Heterobasidion and related genera (Fig. 3).
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Using the T. versicolor gene Tv-pgv as an outgroup, there was bootstrap support (74%) for grouping the amino-acid sequences of the fragments from Heterobasidion, Bondarzewia, Amylostereum, and Echinodontium (Fig. 4), and this clade was found in each of the 60 most-parsimonious trees (Fig. 5). The fragments cloned from species of Amylostereum, Bondarzewia and Echinodontium were distinct from those in Heterobasidion and were designated as mnpA to mnpE, but the B. montana mnp2 and the mnp2 gene of Heterobasidion formed a clade with strong (86%) bootstrap support (Fig. 4). The fragment from E. tsugicola mnpE and the fragment from A. laevigatum mnpC appear to be related (Figs. 4 and 5). Among the Heterobasidion fragments, there was bootstrap support for the branches of each of the four identified genes and for the branch containing mnpA fragments identified in Amylostereum and Echinodontium (Tabata et al 2000). Although the various taxa of Heterobasidion tended to have unique amino-acid sequences for each of the putative MnP genes, there was relatively little variation at this level, and most of the branches within the four genes have little or no bootstrap support (Fig. 4). Nonetheless, amino-acid sequences of H. annosum isolates from Europe and North America were distinct, and amino acid sequences for mnp2 from H. parviporum, H. abietinum, H. insulare and H. araucariae were unique (Fig. 4). The mnp3 sequences showed similar distinctions, although the sequences of H. insulare and H. araucariae were identical.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and the inferred amino-acid composition of the cloned fragments strongly indicates that we have characterized parts of four distinct, but structurally similar, manganese peroxidase encoding genes in Heterobasidion. Related MnP gene fragments were identified in genera phylogenetically related to Heterobasidion.
Biochemical features of Heterobasidion peroxidases –
Conserved amino acid positions in the fragments produced from Amylostereum, Bondarzewia, Echinodontium, and Heterobasidion follow the pattern found in other fungal LiPs and MnPs. Residues involved in substrate binding and catalysis at the heme-opening channel might be of particular interest, because structural differences are manifested as differences in substrate specificity and catalytic mechanism. Asp183 residue needed for Mn2+-binding (Kishi et al 1996, Sundaramoorthy et al 1997) is present in all cloned and sequenced fragments, except in the mnpB fragment from B. montana. Position 172 in most of the analyzed peroxidase fragments is Ala, whereas, in E. tsugicola mnpE, it is Ser. Trp at position 172 that has been postulated to be involved in binding of veratryl alcohol (VA) (Doyle et al 1998, Timofeevski et al 1999) and thus in the VA-oxidizing activity of these enzymes. The variable amino acids present at position 172 in our amplified fragments, and the presence of Asp-residue at position 183, required for Mn-ion binding in MnPs, support the idea that the cloned fragments are from genes encoding MnP without VA-oxidizing activity.
Evolution of MnP genes in Heterobasidion and related genera –
The identical intron positioning in the MnP fragments and the high similarity of the genomic MnP sequences indicate close relatedness of Amylostereum, Bondarzewia, Echinodontium and Heterobasidion, consistent with the previous grouping of these genera, referred to as "Group 2" based on nuclear rDNA and mitochondrial rDNA sequences (Hibbett and Donoghue 1995, Hibbett et al 1997). The similarity of the amino-acid sequences of Heterobasidion mnp2 and one of the fragments of B. montana, in particular, suggests a close relationship between these two genera and supports the placement of Heterobasidion in the Bondarzewiaceae. The MnP genes (Tv-mnp2, Tv-mpg1, and Tv-pgv) of the polypored fungus Trametes versicolor show the closest relationship to amino-acid sequences of the MnP genes of Heterobasidion and relatives. Our interpretation of these data is that the so-called "Group 2" genera split long ago from Trametes and that there has been considerable MnP gene duplication since that split.
Previous DNA sequencing of the internal transcribed (ITS) and intergenic spacer regions (IGS) of rDNA (Harrington et al 1998, Harrington and Rizzo 1999) have not differentiated European S-type and F-type groups, and these together were grouped with Asian and North American isolates as a "fir" lineage within H. annosum (Harrington et al 1998). However, differences in RAPD (La Porta et al 1997) and isozyme markers (Karlsson and Stenlid 1991, Otrosina et al 1993) indicated that S- and F-type isolates in Europe were distinct. Mating type tests also have shown that European S and F types were infertile only partially (Korhonen et al 1992, 1997). Although these populations form an unresolved polytomy in mnp1a gene sequences, S and F types from Europe differed in the inferred amino-acid sequences of the other peroxidase genes. The Asian and North American isolates of the F-type had the same inferred amino-acid sequences of the S type, now recognized as H. parviporum. To date, all F-type (now H. abietinum) isolates have been from southern Europe. Failure of rDNA spacer sequences to separate closely related species that are sympatric has been noted in Heterobasidion and Ceratocystis (Harrington and Rizzo 1999, Witthuhn et al 2000). The identical rDNA spacer regions in European H. parviporum and in H. abietinum might have resulted from rare hybridization events in Europe, and along with the concerted evolution and homogenization of the nuclear ribosomal genes, only one of the parental rDNA types has emerged.
Asia appears to be the center of diversity for the genus Heterobasidion, and it has been speculated (Harrington et al 1998) that Asia or Australasia is the center of origin. Heterobasidion parviporum is the only species found in Europe, Asia and North America and shows the greatest diversity in rDNA and peroxidase sequences. Thus far, we have been able to amplify both mnp1a and mnp1b sequences only in H. parviporum. One of many interpretations of these data is that the Heterobasidion ancestor had both mnp1a and mnp1b, and lineage sorting has resulted in the other derived species having either of the two genes. Most of the sequence diversity in peroxidase amino-acid sequences and in rDNA is found in H. parviporum populations from Asia and North America, and either of these two continents might have served as the origin of H. parviporum (Harrington et al 1998).
Because of the limited variation at the amino-acid level and the relatively small number of isolates studied, it is difficult to infer phylogenetic relationships among the Heterobasidion species. The presence of mnp1a and mnp1b in H. parviporum, but only mnp1a in H. abietinum, might be explained by an early splitting of H. abietinum from H. parviporum (Korhonen et al 1997, Harrington et al 1998), with the loss of the mnp1b paralog in H. abietinum. This split might have occurred in eastern Asia, with H. abietinum following a southerly route on Abies hosts and H. parviporum migrating later from Asia to Europe along the more northerly Picea abies/Abies sibirica host route to Europe (Korhonen et al 1997). Although H. abietinum is known only in Europe, analysis of peroxidase amino-acid data and the data from the rDNA spacer regions (Harrington et al 1998, Harrington and Rizzo 1999) is consistent with an Asian origin of the species (Korhonen et al 1997).
The identification of only mnp1a in the European form of H. annosum and only mnp1b in the American form of H. annosum further questions whether these two "pine" lineages are one species (Harrington et al 1998). Both ITS and IGS rDNA analyses fail to group these two geographically isolated populations (Harrington et al 1998, Harrington and Rizzo 1999). The low level of interfertility between European and American H. annosum isolates (Harrington et al 1989) further suggests that they represent distinct species.
The DNA and amino-acid sequences of ecologically important genes, such as the genes coding for lignin-degrading enzymes in white-rot fungi, present tremendous opportunity for inferring phylogenies. Such approaches, however, are hindered by the complexities of gene duplications, variation in sequences among alleles and lineage sorting. With the genus Heterobasidion, we have a relatively small group of well-characterized species with a well-known ecology and biogeography. Using degenerative primers, a unique class of MnP genes was identified in this genus and in related genera, and the amino acid sequences of these genes, although highly conserved, have proven superior to sequences of the rDNA-spacer regions in separating the recently diverged H. parviporum and H. abietinum. Analyses of the DNA sequences of these individual peroxidase genes with a larger sample of isolates should allow further insight into the evolutionary history of this genus.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Accepted for publication July 1, 2002.
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LITERATURE CITED |
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