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School of Forestry, University of Montana, Missoula, Montana 59812
Thomas C. Harrington
Joseph Steimel
Douglas McNew
Department of Plant Pathology, 351 Bessey Hall, Iowa State University, Ames, Iowa 50011
T. D. Paine
Department of Entomology, University of California, Riverside, California 92521
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ABSTRACT |
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Morphology, mitochondrial DNA (mtDNA) restriction fragment polymorphisms (RFLPs) and nuclear DNA (nDNA) fingerprinting were used to clarify relationships among the morphologically similar Ophiostoma and Leptographium species associated with mycangia of three Dendroctonus bark beetles (Ophiostoma clavigerum associated with both D. ponderosae and D. jeffreyi, and L. pyrinum associated with D. adjunctus), as well as a closely related nonmycangial bark beetle associate (L. terebrantis). Most isolates of O. clavigerum form long (40–70 µm), septate conidia, while all isolates of L. terebrantis and L. pyrinum form conidia less than 17.0 µm in length. The conidia of L. pyrinum are pyriform, with truncate bases, while the conidia of the other species form only slightly truncate bases. Conidial masses of L. terebrantis are creamy yellow, while the conidial masses of the other species are white. Nuclear DNA fingerprints resulting from probing PstI restrictions with the oligonucleotide probe (CAC)5 and HaeIII and MspI restrictions of mtDNA, exhibited three major clusters. In the dendrogram developed from mtDNA RFLPs, the L. pyrinum isolates formed one cluster, while the majority of O. clavigerum isolates, including all D. jeffreyi isolates, formed another. A third cluster was composed of all L. terebrantis isolates, as well as several O. clavigerum isolates from D. ponderosae. The inclusion of some O. clavigerum isolates in the L. terebrantis cluster suggests that horizontal transfer of mtDNA has occurred among these fungi. The nDNA dendrogram also exhibited three clusters, and most isolates of L. pyrinum, L. terebrantis and O. clavigerum grouped separately; however, one isolate of O. clavigerum grouped with the L. terebrantis isolates, while one isolate of L. terebrantis grouped with O. clavigerum. No genetic markers were found that distinguished between O. clavigerum associated with D. ponderosae and O. clavigerum associated with D. jeffreyi. Ophiostoma clavigerum might be a recently diverged morphological variant of L. terebrantis, with special adaptations for grazing by young adults of D. jeffreyi and D. ponderosae. The anamorph of O. clavigerum, Graphiocladiella clavigerum, is transferred to Leptographium.
Key words: Dendroctonus adjunctus, D. jeffreyi, D. ponderosae, DNA fingerprinting, Leptographium pyrinum, L. terebrantis, mitochondrial DNA, mycangial fungi, Ophiostoma clavigerum, RFLP, Scolytidae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and apparently are dependent wholly on the host beetle for dispersal. Likewise, the beetles appear to be dependent upon at least some mycangial fungi for successful development and reproduction (Whitney 1971, Barras 1973, Bridges 1983, Goldhammer et al 1990, Coppedge et al 1995, Six and Paine 1998, Ayres et al 2000).
Among the many ascomycetes associated with Dendroctonus mycangia are several blue-staining fungi in the genus Ophiostoma H. & P. Sydow and the asexual genus Leptographium Lagerb. & Melin. (many species of Ophiostoma possess Leptographium anamorphs) (Harrington 1988). Dendroctonus jeffreyi Hopkins and D. ponderosae Hopkins carry Ophiostoma clavigerum (Robinson-Jeffrey & Davidson) Harrington in their mycangia (Whitney and Farris 1970, Six and Paine 1997), while D. adjunctus Blandford carries Leptographium pyrinum Davidson (Six and Paine 1996). The anamorph of Ophiostoma clavigerum and L. pyrinum are similar but morphologically distinct, and the two fungi exhibit high genetic identity with one another based on isozyme markers (Zambino and Harrington 1992, Six and Paine 1999a). Leptographium terebrantis also is similar morphologically to the anamorph of O. clavigerum; it has been isolated from many species of Pinus across North America and from a number of bark beetles, including D. valens LeConte, D. terebrantis (Oliv.) and Hylurgops porosus (LeConte), but it has not been found associated with beetle mycangia (Harrington 1988). Many Ophiostoma and Leptographium species exhibit a high degree of pleomorphism (Malloch and Blackwell 1993), and Tsuneda and Hiratsuka (1984) found a wide range in conidiophore and conidial morphology in O. clavigerum. This, and the high degree of similarity in isozyme phenotypes, led Zambino and Harrington (1992) to suggest that O. clavigerum, L. pyrinum, L. terebrantis and some other Leptographium species may be morphological variants of a single species.
Some uncertainty also exists whether O. clavigerum associated with D. jeffreyi and O. clavigerum associated with D. ponderosae constitute a single species or comprise a pair of cryptic species or physiologic races. No differences were seen in O. clavigerum isolates from the mycangia of the two beetles using morphology, isozymes or temperature tolerances (Six and Paine 1997). This fungus, however, when isolated from the two beetles, exhibits significant differences in tolerances for host tree-resin components, with greater tolerances for host resins than non-host resins when grown in artificial culture (Paine and Hanlon 1994). Ophiostoma clavigerum associated with the two beetles also exhibited differential growth in bolts of Pinus contorta Dougl. and P. jeffreyi Grev. & Balf., hosts of D. ponderosae and D. jeffreyi, respectively (Six and Paine 1998). Dendroctonus jeffreyi and D. ponderosae are sibling species that are morphologically and genetically very similar (Higby and Stock 1982, Wood 1982). However, there is no overlap in host tree species used by the two beetle species. Dendroctonus jeffreyi is monophagous and attacks only P. jeffreyi (Wood 1982). Dendroctonus ponderosae is polyphagous, attacking 13 species of Pinus but not P. jeffreyi (Wood 1982). The major resin components of the host trees of the two beetles differ considerably. n-Heptane is the major resin component of P. jeffreyi, while the main resin components of hosts of D. ponderosae are monoterpenes and resin acids (Mirov 1929, Smith 1967, Anderson et al 1969). Therefore, O. clavigerum associated with D. jeffreyi and O. clavigerum associated with D. ponderosae are isolated in different chemical environments, which ultimately may result in divergence due to selection and random genetic drift. Divergence in morphologically simple fungi may result in genetic differentiation without concurrent morphological changes (Kemp 1977, Brasier 1986).
Our objectives were (1) to assess whether L. pyrinum is a species distinct from O. clavigerum or simply a morphologic variant, (2) to determine whether differentiation is occurring between O. clavigerum associated with D. jeffreyi and O. clavigerum associated with D. ponderosae and (3) to assess the relationship of the nonmycangial L. terebrantis to O. clavigerum and L. pyrinum. In addition to morphological comparisons, we used nuclear DNA (nDNA) fingerprinting and restriction fragment-length polymorphisms (RFLPs) of mitochondrial DNA (mtDNA), techniques that have been used successfully to differentiate among species and strains of several fungi (Meyer et al 1991, DeScenzo and Harrington 1994).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Ophiostoma clavigerum was isolated from D. ponderosae (DP) collected at three locations in California (isolates C836, C837, C838, C839 and C841) where D. ponderosae and D. jeffreyi are sympatric. Ophiostoma clavigerum also was isolated from D. jeffreyi (DJ) collected at 10 California sites that are representative of a majority of the geographic range of that beetle. In most, if not all, of these locations, D. jeffreyi and D. ponderosae are sympatric (Wood 1982). Fungi from allopatric populations of D. ponderosae also were included for comparison (C295, C293 and C86).
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Total genomic DNA extraction. Mycelia were grown in 25 mL liquid medium (2% malt extract, 0.2% yeast extract) in 125 mL Erlenmeyer flasks and held at room temperature (ca 21 C) in the light. After 14 d the mycelial mats were collected and dried with vacuum filtration through 1 mm Whatman No. 1 filter paper (Whatman International Ltd., Kent, England). The mats were placed between paper towels and dried for an additional 10 min. Immediately after drying, the mats were ground with mortar and pestle to a fine powder in liquid nitrogen.
Total genomic DNA extractions were carried out with the ground mycelia and a modification of the method developed by Dellaporte et al (1983) and detailed in DeScenzo and Harrington (1994).
mtDNA RFLPs –
RFLPs of mtDNA can be visualized directly from stained gels of total genomic DNA that has been digested with restriction enzymes possessing G-C, four-base recognition sites (Wingfield et al 1996). mtDNA exhibits a high degree of restriction fragment-length polymorphism at the intraspecific level, and length mutations have been shown to be the major cause of this variation (Sanders et al 1977, Taylor et al 1986, Bruns et al 1988). Total genomic DNA was digested with HaeIII and MspI restriction enzymes (Promega, Madison, Wisconsin), which recognize the base sequences GGCC and CCGG, respectively. These enzymes digest the majority of nuclear DNA to relatively short lengths, leaving relatively long pieces of AT-rich DNA, which are primarily from the mitochondrial genome. After electrophoresis, ethidium bromide-stained bands of uniform intensity are scored as mtDNA bands. Protocols used for electrophoresis and staining of RFLPs were developed by Wingfield et al (1996). mtDNA RFLPs were not obtained for isolates C186, C847 and DLS568, and nDNA fingerprints were not obtained for isolate 608.
nDNA fingerprinting. nDNA fingerprints are produced by the hybridization of DNA probes (oligonucleotides) to restriction fragments of genomic DNA. These probes are homologous to hypervariable repetitive sequences often called "simple repetitive sequences" or "microsattelite DNAs". These simple repetitive sequences often exhibit substantial variability in their repeat copy number for a given locus.
For nDNA fingerprinting, total genomic DNA was digested using the restriction enzyme PstI (Promega, Madison, Wisconsin) and then hybridized with the synthetic oligonucleotide probe (CAC)5. This probe has been shown to be useful in detecting variation in both basidiomycetes and ascomycetes (DeScenzo and Harrington 1994). Protocols for PstI digestion, electrophoresis, radiolabeling, in-gel hybridization and autoradiography are described in DeScenzo and Harrington (1994).
Data analysis –
Band sizes for both mtDNA RFLPs and nDNA fingerprints were determined using Gelreader (version 2.0.5) (National Center for Supercomputing Applications 1991). Bands of the same molecular weight were scored as alleles possessing two character states (presence/absence). Gels used for DNA fingerprinting were run twice, and only bands distinct and scorable in both runs were analyzed.
Cluster analysis was performed using the GENDIST (Nei's genetic distance) and NEIGHBOR (UPGMA, unweighted pair-group method with arithmetic averaging) programs found within the PHYLIP package (version 3.5) (Felsenstein 1993). Trees were produced from PHYLIP files using TREEVIEW (version 1.6.6.) (Page 1996).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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nDNA fingerprinting – Fewer phenotypes were expressed in the nDNA fingerprints compared with the number of phenotypes observed with mtDNA RFLPs. The nDNA fingerprint of the four groups of fungi probed with the (CAC)5 oligonucleotide is shown in Fig. 20.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The mtDNA RFLPs and nDNA fingerprints provided additional evidence that L. pyrinum is a good species and not a morphologic variant of O. clavigerum. However, evidence for the separation of L. terebrantis and O. clavigerum was not so strong. Most isolates of L. terebrantis and O. clavigerum clustered in agreement with the morphology consistent for their respective species in the dendrograms produced from mtDNA RFLPs and nDNA fingerprints. In each case, however, inconsistencies were seen. A possible explanation for these inconsistencies is that the two fungi actually comprise a single species that exhibits morphological variation linked to its ecology (mycangial versus nonmycangial). One the other hand, the two fungi might be distinct species that recently have diverged but, because of lineage sorting, are not clearly separable using these genetic markers.
Leptographium terebrantis is loosely associated with bark beetle species in several genera (Harrington 1988), while O. clavigerum has been found only with D. ponderosae (Whitney and Farris 1970) and the closely related D. jeffreyi (Six and Paine 1997) and L. pyrinum only with D. adjunctus (Six and Paine 1996). Furthermore, the unusually long septate and clavate-shaped conidia and large spreading conidiophores of O. clavigerum might be derived characters related to ambrosial feeding by the associated beetles. Young adults are known to feed on dense sporogenous fungal growth in pupal chambers for several weeks before emergence from the natal host tree. In addition to the large conidia and spreading conidiophores, O. clavigerum produces smaller and less elaborately branched conidiophores and smaller conidia (Tsuneda and Hiratsuka 1984) that are morphologically very similar to those produced by L. terebrantis. Thus, while O. clavigerum may have retained the conidium and conidiophore morphology of L. terebrantis, it also produces a conidium and conidiophore type especially suitable for ambrosial feeding by young adult beetles. We can speculate that L. terebrantis might be the more primitive of the three species and that O. clavigerum and L. pyrinum might well have diverged from L. terebrantis when they developed close mycangial associations with specific bark beetles.
Microscopic examination of the conidia and conidiophores of the isolates studied for genetic markers showed three morphological groups that generally showed agreement with the clustering based on nDNA fingerprinting. That is those isolates that produced short, truncate conidia were in the L. pyrinum cluster; those that produced long, clavate conidia, often with one or two septations, tended to group in the O. clavigerum cluster. Further, the broad, spreading fasicles of conidiophores typical of O. clavigerum were seen in isolates of the O. clavigerum cluster but not in isolates in the L. terebrantis cluster. The two notable exceptions are isolates C25 and C813. The former isolate originally was identified as L. terebrantis in Harrington and Cobb (1983) but was found to produce clavate conidia in a later study (Zambino and Harrington 1992), in which it was referred to as O. clavigerum. Our more recent examinations of this strain revealed no clavate conidia, but the broad, spreading conidiophores typical of O. clavigerum were seen. The insect associate of C25 is not known, but C25 was isolated from Pinus contorta, which is a host of L. terebrantis and O. clavigerum and of the bark beetles, D. valens and D. ponderosae, that vector these fungi,. Placement of C25 in the O. clavigerum cluster based on nDNA fingerprinting would suggest that C25 is O. clavigerum, but the culture has deteriorated and no longer produced the clavate conidial state, a deterioration that has been noted in other cultures of O. clavigerum (Tsuneda and Hiratsuka 1984). The other exceptional isolate is C813, which continues to produce large (55–65 µm), clavate conidia and broad, spreading conidiophores. Thus, C813 is morphologically O. clavigerum, though it was isolated from D. valens (rather than D. ponderosae) and it clusters with L. terebrantis based on nDNA fingerprints. Isolate C813 might be an intermediate in an ongoing process of speciation. It also might be that these two species are not genetically isolated, which also might be suggested by the mtDNA data.
A possible explanation for the resolution of five O. clavigerum (DP) associates in the L. terebrantis cluster in the dendrogram developed from the mtDNA RFLPs is that after the divergence of L. terebrantis and O. clavigerum, there has been horizontal transfer of mtDNA, but not nDNA, between the two species. The horizontal transfer of mtDNA in fungi remains poorly understood, and the mechanisms involved are unknown. The occurrence of such transfers of mtDNA has been suggested in other fungi infecting trees (Brasier et al 1993, Harrington et al 1998). It is interesting to note that no isolates of O. clavigerum (DJ) showed evidence of possessing mtDNA polymorphisms typical of L. terebrantis. This might be due to a lack of contact between O. clavigerum (DJ) and L. terebrantis in P. jeffreyi. D. valens, a vector of L. terebrantis, can be found commonly in pines colonized by D. ponderosae and O. clavigerum (DP), and L. terebrantis might interact in such trees. D. valens also attacks the bases of P. jeffreyi attacked by D. jeffreyi; however, it is not known how well L. terebrantis is able to colonize tissues of this tree. P. jeffreyi is quite different chemically than other pines and limits the growth of some ophiostomatoid fungi (Paine and Hanlon 1994, Six and Paine 1998). If growth of L. terebrantis is poor in P. jeffreyi, Ophiostoma clavigerum (DJ) might interface only rarely, or not at all, with this fungus.
On the other hand, the patterns we observed might suggest incomplete lineage sorting accompanied by limited morphological divergence, which can indicate recent or incomplete speciation events (Flowers and Folz 2001). However, this explanation still does not clarify the inconsistencies found using the nDNA probe (CAC)5.
About half of the described Leptographium species have Ophiostoma teleomorphs, but the others, including L. pyrinum and L. terebrantis, are known only by their anamorphs (Harrington 1988, Jacobs and Wingfield 2001) and may be strictly asexual. The mode of reproduction (asexual or sexual) should not affect variation or polymorphism of mtDNA. However, variation and polymorphism of nDNA is predicted to be lower in asexual species than in sexual species. In this study, Leptographium species possessed as high or higher nuclear genetic variation than did the sexually reproducing Ophiostoma clavigerum. Ophiostoma clavigerum possessed the lowest genetic variation and was the least polymorphic of all fungi studied. These results concur with results of a study assaying genetic variation in O. clavigerum (DJ) using isozymes, which revealed little genetic variation and polymorphism in this fungus (Six and Paine 1999b).
The low genetic variability in O. clavigerum relative to the asexual Leptographium species may indicate that sexual reproduction in this species is uncommon. We have not observed the sexual state of O. clavigerum in nature, nor have we been able to produce it in artificial culture despite numerous pairings of isolates in the laboratory (Six and Paine 1997, T. C. Harrington unpubl, D. L. Six unpubl). The only known observations of ascomata for O. clavigerum were reported in a pair of related studies by Robinson (1962) and Robinson-Jeffrey and Davidson (1968) in which the authors observed neckless perithecia (unusual for Ophiostoma species) in sapwood and, more rarely, in culture.
The genus Graphiocladiella was erected for Leptographium-type species with individual conidiophores to those clustered into a synnema-like group (Upadhyay 1981). However, in all other respects these fungi appear to be Leptographium species (Harrington et al 2001), and O. clavigerum is clearly closely related to other Leptographium species. Thus we propose to transfer this anamorph to Leptographium.
Ophiostoma clavigerum (Robinson.-Jeff. & Davids.) Harrington, Mycotaxon 28: 41. 1987.
Anamorph. Leptographium clavigerum (Upad.) Harrington, Six et McNew, comb. nov. 
Graphiocladiella clavigerum Upad. Monogr. Ceratocystis and Ceratocystiopsis, p. 138, 1981.
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FOOTNOTES |
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Accepted for publication February 6, 2003.
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LITERATURE CITED |
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Ayres MP, Wilkens RT, Ruel JJ, Lombardero MJ, Vallery E., 2000 Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi (Coleoptera: Scolytidae). Ecology 81:2198-2210
Barras SJ., 1973 Reduction of progeny and development in the southern pine beetle following removal of symbiotic fungi. Can Entomol 105:1295-1299
Brasier CM., 1986 The dynamics of fungal speciation. In: Raynor ADM, Brasier CM, Moore D, eds. Evolutionary biology of the fungi. Cambridge, Massachusetts: Cambridge University Press. p 231–260
Brasier CM., Bates MR, Charter NW, Buck KW., 1993 DNA polymorphism, perithecial size and molecular aspects of D factors in Ophiostoma ulmi and O. novo-ulmi. In: Sticklen MB, Sherald JL, eds. Dutch elm disease research-cellular and molecular approaches. New York: Springer-Verlag. p 308–321
Bridges JR., 1983 Mycangial fungi of Dendroctonus frontalis (Coleoptera: Scolytidae) and their relationship to beetle population trends. Environ Entomol 12:858-861
Bruns TD, Palmer JD, Shumard DS, Grossman LI, Hudspeth MES., 1988 Mitochondrial DNAs of Suillus: threefold size change in molecules that share a common gene order. Curr Genet 13:49-56[Medline]
Coppedge BR, Stephen FM, Felton GW., 1995 Variation in female southern pine beetle size and lipid content in relation to fungal associates. Can Entomol 127:145-154
Dellaporte SL, Word J, Hicks JB., 1983 A plant DNA minipreparation. Version II. Plant Mol Biol Rep 1:19-21
DeScenzo RA, Harrington TC., 1994 Use of (CAT)5 as a DNA fingerprinting probe for fungi. Phytopathology 84:534-540
Felsenstein J., 1993 PHYLIP 3.5. Software and user manual. Seattle, Wash.: University of Washington
Flowers JM, Folz DW., 2001 Reconciling molecular systematics and traditional taxonomy in a species-rich clade of sea stars (Leptasterias subgenus Hexasterias). Marine Biol 139:475-483
Goldhammer DS, Stephen FM, Paine TD., 1990 The effect of the fungi Ceratocystis minor (Hedgecock) Hunt, Ceratocystis minor (Hedgecock) Hunt var. Barrasii Taylor, and SJB 122 on reproduction of the southern pine beetle, Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae). Can Entomol 122:407-418
Harrington TC., 1988 Leptographium species, their distributions, hosts and insect vectors. In: Harrington TC, Cobb FW. Jr, eds. Leptographium root diseases on conifers. St. Paul, Minnesota: APS Press. p 1–39
Harrington TC., Cobb FWJr., 1983 Pathogenicity of Leptographium and Verticicladiella spp. isolated from roots of western North American conifers. Phytopathology 73:596-599
Harrington TC., Steimel J, Kile G., 1998 Genetic variation in three Ceratocystis species with outcrossing, selfing and asexual reproductive strategies. European J For Path 28:217-226
Harrington TC., McNew D, Steimel J, Hofstra D, Farrell R., 2001 Phylogeny and taxonomy of the Ophiostoma piceae complex and the Dutch elm disease fungi. Mycologia 93:111-136
Higby PK, Stock MW, 1982 Genetic relationships between two sibling species of bark beetle (Coleoptera: Scolytidae), Jeffrey pine beetle and mountain pine beetle, in northern California. Ann Entomol Soc Amer 75:668-674
Jacobs K, Wingfield MJ., 2001 Leptographium species. Tree pathogens, insect associates and agents of blue-stain. St. Paul, Minnesota: APS Press. 207 p
Kemp RFO, 1977 Oidial homing and the taxonomy and speciation of basidiomycetes with special reference to the genus Coprinus. In: Clemencon H, ed. The species concept in Hymenomycetes. Vaduz Cramer. p 259–273
Malloch D, Blackwell M., 1993 Dispersal biology of the ophiostomatid fungi. In: Wingfield MJ, Seifert KA, Webber JF, eds. Ceratocystis and Ophiostoma: taxonomy, ecology, and pathogenicity. St. Paul, Minnesota: APS Press. p 195–206
Meyer W, Koch A, Niemann C, Beyermann B, Epplen JT, Borner T., 1991 Differentiation of species and strains among filamentous fungi by DNA fingerprinting. Curr Genet 19:239-242[Medline]
Mirov NT., 1929 Chemical analysis of the oleoresins as a means of distinguishing Jeffrey pine and western yellow pine. J Forest 27:176-187
National Center for Supercomputing Applications. 1991 . Gelreader version 2.0.5, Urbana-Champaign: University of Illinois
Page RDM., 1996 TREEVIEW: an application to display phylogenetic trees on personal computers. Computer applications in the Biosciences 12:357-358
Paine TD, Hanlon CC., 1994 Influence of oleoresin constituents from Pinus ponderosa and Pinus jeffreyi on the growth of mycangial fungi from Dendroctonus ponderosae and Dendroctonus jeffreyi. J Chem Ecol 20:2551-2563
Robinson RC., 1962 Blue stain fungi in lodgepole pine (Pinus contorta Dougl. var. latifolia Engelm.) infested by the mountain pine beetle (Dendroctonus monticolae Hopk). Can J Bot 40:609-614
Robinson-Jeffrey RC, Davidson RW., 1968 Three new Europhium species with Verticicladiella imperfect states on blue-stained pine. Can J Bot 46:1523-1527
Sanders JPM, Heyting C, Verbett MP, Meijlink F, Borst P., 1977 The organization of genes in yeast mitochondrial DNA. III. Comparison of the physical maps of the mitochondrial DNAs from three wild-type Saccharomyces strains. Mol Gen Genet 157:239-261
Six DL, Paine TD., 1996 Leptographium pyrinum is a mycangial fungus of Dendroctonus adjunctus. Mycologia 88:739-744
Six DL, Paine TD., 1997 Ophiostoma clavigerum is the mycangial fungus of the Jeffrey pine beetle, Dendroctonus jeffreyi (Coleoptera: Scolytidae). Mycologia 89:858-866
Six DL, Paine TD., 1998 Effects of mycangial fungi and host tree species on progeny survival and emergence of Dendroctonus ponderosae (Coleoptera: Scolytidae). Environ Entomol 27:1393-1401
Six DL, Paine TD., 1999a Phylogenetic comparison of ascomycete mycangial fungi and Dendroctonus bark beetles (Coleoptera: Scolytidae). Ann Entomol Soc Amer 92:159-166
Six DL, Paine TD., 1999b Allozyme diversity and gene flow in Ophiostoma clavigerum (Ophiostomatales: Ophiostomataceae), the mycangial fungus of the Jeffrey pine beetle, Dendroctonus jeffrey (Coleoptera: Scolytidae). Can J For Res 29:324-331
Smith RH., 1967 Variations in the monoterpene composition of the wood resin of Jeffrey, Washoe, Coulter, and lodgepole pines. For Sci 13:247-252
Taylor JW, Smolich BD, May G., 1986 Evolution and mitochondrial DNA in Neurospora crassa. Evolution 40:716-739
Tsuneda A, Hiratsuka Y., 1984 Sympodial and annelidic conidiation in Ceratocystis clavigera. Can J Bot 62:2618-2624
Upadhyay HP., 1981 A monograph of Ceratocystis and Ceratocystiopsis. Athens, Georgia: The University of Georgia Press. 176 p
Whitney HS., 1971 Association of Dendroctonus ponderosae (Coleoptera: Scolytidae) with blue-stain fungi and yeasts during brood development in lodgepole pine. Can Entomol 103:1495-1503
Whitney HS., Farris SH., 1970 Maxillary mycangium in the mountain pine beetle. Science 167:54-55
Wingfield BD, Harrington TC, Steimel J., 1996 A simple method for detection of mitochondrial DNA polymorphisms. Fungal Genet Newsletter 43:56-60
Wood SL., 1982 The bark and ambrosia beetles of North and Central America (Coleoptera: Scolytidae), a taxonomic monograph. Great Basin Natur Mem 6
Zambino PJ, Harrington TC., 1992 Correspondence of isozyme characterization with morphology in the asexual genus Leptographium and taxonomic implications. Mycologia 84:12-25
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