| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
0 111 Koshland Hall, College of Natural Resources, University of California at Berkeley, Berkeley, California 94720-3102, USA
Received for publication June 15, 1999. Accepted for publication September 7, 1999.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSION LITERATURE CITED |
|---|
Key Words: Abies magnifica • community structure • mutualism • mycoheterotrophy • parasitism • Rhizopogon ellenae • tripartite symbiosis
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSION LITERATURE CITED |
|---|
). Like all other monotropes, the snow plant is a mycoheterotroph: a nonphotosynthetic plant that obtains its fixed carbon from fungi. This is a successful lifestyle as evidenced by over 400 known species in 87 genera, notably in the families Ericaceae and Orchidaceae (Leake, 1994
). Many mycoheterotrophs examined to date are linked to surrounding trees via a shared ectomycorrhizal (ECM) fungus (Furman and Trappe, 1971
; Vreeland, Kleiner, and Vreeland, 1981
; Cullings, Szaro, and Bruns, 1996
; Taylor and Bruns, 1997
). This interaction is called "epiparasitism" because the mycoheterotroph indirectly parasitizes the trees (Björkman, 1960
), thus cheating the ECM mutualism. Furthermore, some ECM photosynthetic angiosperms are now known to engage in facultative epiparasitism. Simard et al. (1997a, b)
demonstrated that in nature carbon can be derived from the better competitor tree species by a poorer one if both are colonized by common ECM fungi, thereby providing a novel mechanism for overcoming competitive exclusion. It appears that by permanently reversing carbon flow in their favor, nonphotosynthetic epiparasites have evolved to one extreme along a continuum of plant strategies for carbon acquisition.
Extreme host specialization appears to be a general pattern among nonphotosynthetic epiparasites; this contrasts with photosynthetic plants, which typically form mycorrhizas with phylogenetically diverse fungi. Recent studies have shown that some epiparasitic orchids (Taylor and Bruns, 1997
) and monotropes (Cullings, Szaro, and Bruns, 1996
; C. K. Lefevre, and R. Molina, personal communication, Oregon State University) specialize on highly restricted sets of closely related ECM fungal hosts. In fact, the only exception to this pattern of specialization was the snow plant, which appeared to be a generalist (Cullings, Szaro, and Bruns, 1996
). However, we have recently determined that the snow plant is specialized over a large area of the Sierra Nevada of California on the ECM fungus Rhizopogon ellenae A. H. Smith (Bidartondo, Kretzer, and Bruns, 1998
), a member of the suilloid lineage of the Boletales (Bruns et al., 1998
). Over its entire range, the snow plant may actually form a "geographic mosaic of specialization" (Thompson, 1994
).
Although we follow Björkman (1960)
in referring to the monotropes as epiparasites, a net cost to either the photosynthetic plant or the fungal associate remains to be shown (Leake, 1994
). Epiparasitism is consistent with (a) the heterotrophic habit of the monotropes; (b) the fact that extreme specialization is a common characteristic of parasitic systems (Price, 1980
; Thompson, 1994
); and (c) evidence for flow of 14C-labeled glucose from trees to Monotropa hypopitys L. (Ericaceae), a close relative of Sarcodes (Björkman, 1960
). However, Björkman also found that the growth of a fungus isolated from Monotropa mycorrhizas was greatly stimulated by an extract of the plant. Miller and Allen (1992)
speculate that potential ecophysiological benefits for trees of supplying carbon to Monotropa may render the association mutualistic. Research on monotrope symbioses has focused on the mycoheterotrophic plant's nutrition (Björkman, 1960
), mycorrhizal ultrastructure (Duddridge and Read, 1982
; Robertson and Robertson, 1982
), germination (Francke, 1934
; S. McKendrick, personal communication, University of Sheffield), flowering (D. Luoma, personal communication, Oregon State University), and associated fungi (Cullings, Szaro, and Bruns, 1996
). However, little is known about basic ecological traits of monotropes, and this is partly responsible for our difficulties in understanding the nature of their interactions.
In this study, we investigated the ECM community of a red fir, Abies magnifica Andr. Murray (Pinaceae), forest where the snow plant flowers abundantly, and we asked what part R. ellenae played in this community. Although one might expect that the specialization of the snow plant on R. ellenae would result in spatial correlation between these two organisms in nature, at least five different ECM root distributions might be expected: (1) R. ellenae could be free of snow plant infection in localized regions of a site where snow plants are present; (2) R. ellenae could be negatively spatially correlated with the snow plant; (3) R. ellenae could be positively spatially correlated with the snow plant; (4) R. ellenae could be uniformly abundant at a site and randomly associated with the snow plant (particularly since Rhizopogon species form rhizomorphs well suited for long-distance physiological transport); (5) R. ellenae ECM roots could be low in abundance and randomly distributed. Low abundance was suggested for Rhizopogon subcaerulescens A. H. Smith (Boletaceae) ECM roots with respect to rootballs of the monotrope Pterospora andromedea Nutt. (Ericaceae) (Cullings, Szaro, and Bruns, 1996
). Furthermore, low abundance is predicted for suilloid fungi, such as Rhizopogon Fr. species, which are known to fruit profusely while making comparatively few connections to trees, and thus are hypothesized to have higher carbon sink strengths than other ECM fungi (Danielson, 1984
; Natarajan, Mohan, and Ingleby, 1992
; Gardes and Bruns, 1996
). To test these hypotheses, we examined the distribution of red fir ECM roots within snow plant rootballs and at several distances from snow plant inflorescences.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSION LITERATURE CITED |
|---|
Design
We sampled a total of five snow plants on either 16 July or 20 August 1997 from outside of our circular plots. We selected inflorescences for sampling based on the criterion that they had to be separated by at least 5 m from any other flowering snow plant. Each selected inflorescence became the center for a linear transect. We removed two soil cores at each of four distances (10, 50, 100, and 500 cm) away from each selected inflorescence. Cores removed at 5 m were also at least 5 m away from neighboring snow plant inflorescences. The soil cores were 4.6 cm in diameter and they were as deep as the rocky ground allowed, but at least 20 cm and at most 40 cm. Then we excavated the rootball of each snow plant. The rootball is a congested and dense mass of brittle, succulent, highly branched monotropoid mycorrhizal roots from which adventitious inflorescence axes emerge (Wallace, 1975
). In one case, we were unable to find the rootball in the soil after the inflorescence axis accidentally broke off. All soil cores and rootballs were kept at 4°C and processed within 3 wk of field sampling.
We sprayed each soil core vigorously with tap water over 2 mm and 500-µm mesh stacked sieves to separate coarse and fine soil fractions. The Sarcodes rootballs were manually broken into small pieces and otherwise treated in the same manner. All the washed soil and roots collected in both sieves were spread thinly in petri dishes and examined using stereo microscopes. All Abies roots were collected from each individual core or rootball and sorted into morphotypes according to gross mantle characters (color, color changes, branching pattern, presence of rhizomorphs, mantle surface, thickness). We discarded degraded roots and placed recognizable ECM roots that were partially degraded and/or not turgid in separate morphotypes. We did not attempt to identify identical morphotypes among different cores based on morphological characters alone, but instead relied on molecular analysis to determine identity among samples from different cores. We did not collect the monotropoid mycorrhizas of the snow plant itself for this study. All ECM roots were then lyophilized, and the dry mass of each morphotype was determined. We calculated approximate soil volumes sampled from the core diameter and the soil depth reached. For the rootballs, we determined the volume displaced in water by the snow plant roots after these had been broken up and examined.
Ectomycorrhizal identification
We identified ECM fungi using methods described by Gardes and Bruns (1996)
. Briefly, we extracted DNA from individual ECM roots of each morphotype and we amplified the internal transcribed spacer (ITS) of the nuclear ribosomal repeat by the polymerase chain reaction (PCR) with the fungal-specific primers ITS1F and ITS4B, or ITS1F and ITS4 (White et al., 1990
; Gardes and Bruns, 1993
). PCR products were then screened by restriction fragment length polymorphisms (RFLP) using first the restriction endonuclease (RE) Alu-I (New England Biolabs Inc., Beverly, Massachusetts, USA). When types were redundant within a core by Alu-I RFLP only one of those types was analyzed further. We then screened with the RE Hinf-I. On average, we extracted and amplified each morphotype 2.6 times, with a bias for more abundant types. We estimated the molecular size of the restriction fragments obtained with Alu-I and Hinf-I using the program GelReader v.2.0.5 (National Center for Supercomputing Applications, Champaign, Illinois) and sorted the morphotype fragment sizes in various combinations in Excel 4.0 spreadsheets (Microsoft Co., Redmond, Washington, USA) to identify groups of morphotypes that matched for both restriction endonucleases. We checked that matching morphotypes were compatible according to our descriptions of their gross morphology. From previous studies we knew that ECM roots of closely related Rhizopogon section Amylopogon species are virtually indistinguishable by morphology alone. They are also difficult to differentiate by ITS RFLP with the two restriction enzymes mentioned above. Thus, we digested the ITS PCR products of all Rhizopogon-like types with a third RE, Cfo-I, which differentiates R. ellenae.
Lastly, we examined the phylogenetic distribution of the ITS RFLP groups obtained. Because fungal fruiting at our site is rare and sporadic, direct RFLP matching to fungal sporocarps was not an option. Instead, we ranked ITS RFLP types according to their dry biomass pooled over all samples, and we selected those types with highest biomass for PCR amplification and sequencing of a fragment of the fungal mitochondrial large subunit (mtLSU) rDNA (Bruns et al., 1998
). In most cases, the primer combination ML5/ML6 was used; in cases where PCR amplification was weak, or if sequencing proved difficult possibly due to the presence of introns, we attempted amplification with the primer combinations MLIN5R/ML5, CML5.5/ML6, or MLIN3/ML5.5 (Bruns et al., 1998
). Sequencing of both strands was performed with an ABI model 377 Sequencer (Applied Biosystems Co., Foster City, California, USA) using an ABI PRISMTM Dye Terminator Cycle Sequencing Core Kit (Perkin Elmer Co., Foster City, California, USA) or a Thermo SequenaseTM Dye Terminator Cycle Sequencing Pre-Mix Kit (Amersham Pharmacia Biotech, Piscataway, New Jersey, USA). We used DNA Sequencing Analysis v.2.1.2 and Sequence Navigator v.1.0.1 (Applied Biosystems Co., Foster City, California, USA) for processing raw data. The nearest relatives of each mycorrhizal type were inferred with the neighbor-joining algorithm implemented in the program PAUP*d64 (Swofford, 1993
) using a database by Bruns et al. (1998)
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSION LITERATURE CITED |
|---|
1800 m2, we found a total of 80 different ectomycorrhizal types defined by unique combinations of characters (gross morphology and ITS RFLP). We found 47 ECM types that occurred in single soil cores (59% of all ECM types, 7% of all ECM biomass sampled). For ease of presentation, we pooled the data for soil cores taken at the same distance from each of the five snow plants sampled. Analysis considering each snow plant and its surrounding soil cores as independent units leads to essentially the same conclusions. We identified 28 of the 80 ITS RFLP types to family, genus, or species level, corresponding to 36% of all ECM types and 89% of all ECM biomass sampled. The rest of ECM types are labeled "unknowns." Types labeled "nonamplifying" (2.9% of all ECM biomass sampled) were partially degraded and/or nonturgid types that failed to PCR-amplify after at least three independent DNA extractions and several attempts at PCR of both the ITS and mtLSU regions. The cumulative dry mass of each ITS RFLP type at each distance is shown in Fig. 1. Rhizopogon ellenae is the predominant type in the Sarcodes rootballs and 10 cm away from the inflorescences.
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSION LITERATURE CITED |
|---|
). Despite our Sarcodes sanguinea-biased sampling, we can infer that members of the Russulaceae and Thelephoraceae dominate at distances farthest away from Sarcodes at our study site. These fungal families are also dominant in other pinaceous Californian forests (Gardes and Bruns, 1996
; Horton and Bruns, 1998
; Stendell, Horton, and Bruns, 1999
). The high diversity and patchiness of the ECM community at our site (Fig. 1) resemble that found in a Pinus ponderosa Laws. (Pinaceae) forest located also in the Sierra National Forest (Stendell, Horton, and Bruns, 1999
) as well as in old-growth forests (Dahlberg, Jonsson, and Nylund, 1997
; Jonsson et al., 1999
). In contrast, the ECM community of Pinus muricata (Pinaceae) forests in coastal California appears generally less diverse (Gardes and Bruns, 1996
). The distribution of red fir root tips colonized by R. ellenae at our site was greatest directly on the snow plant rootballs and decreased sharply away from them. This finding suggests that most physiological transfer between snow plant roots and R. ellenae–Abies ECM occurs over short distances (i.e., <10 cm) despite the presence of R. ellenae rhizomorphs, which can exceed that length. It is interesting that another suilloid fungus (Suilloid 1; Fig. 1), which appears more uniformly distributed and ranks fourth overall, does not associate with the snow plant. Rhizopogon ellenae was not detected in any of the nine soil cores we removed 500 cm away from snow plants. Thus, the snow plants sampled appear to occupy dense islands of R. ellenae ECM roots. Despite the unevenness observed, ECM type richness within the snow plant rootballs was not significantly different than that in the surrounding soil when we take into account differences in sampled volume between rootballs and soil cores.
If a fungus is necessary for seed germination (Leake, 1994
), our results are consistent with data indicating that most seeds of the obligate mycoheterotrophs Monotropa hypopithys L. (Ericaceae) and Neottia nidus-avis L. (Rich) (Orchidaceae) germinate close to prerecorded positions of adult plants (S. McKendrick, personal communication, University of Sheffield). Snow plant seeds germinate in the laboratory when grown axenically within R. ellenae cultures, and field germination trials have recently been successful (T. D. Bruns, unpublished data).
Unexpectedly, the snow plant rootballs sampled were sites of disproportionately high concentrations of red fir roots compared to any soil core, and R. ellenae colonized the vast majority of those roots (86–98%; Fig. 2). For the related monotrope, Pterospora andromedea, Cullings, Szaro, and Bruns (1996)
documented the scarcity of ECM roots of its symbiont, Rhizopogon subcaerulescens, in one rootball and in soil cores removed at 0.5 m from three inflorescences. Because the P. andromedea rootball data disagree with our results for Sarcodes rootballs, we examined two additional P. andromedea rootballs. These were densely covered with ECM roots with a morphology consistent with Rhizopogon-Pinus mycorrhizas, similar to what we have observed for Sarcodes.
Two possible explanations exist for the association of Sarcodes with dense clumps of R. ellenae. Either Sarcodes plants preferentially establish in pre-existing clumps, or they create them. We favor the second explanation for two reasons. First, the Sarcodes rootball itself has relatively few ECM roots in it; instead most roots are found on the outside surface. This distribution suggests that Abies–R. ellenae ECM roots form as the Sarcodes rootball develops. If instead Sarcodes roots were finding such clumps and establishing around them, one would expect the Abies–R. ellenae ECM clumps to be predominantly internal to the rootballs. Second, these clumps are much larger than any we have observed for related Rhizopogon species in a variety of pinaceous forests. Most, perhaps all, Rhizopogon species have the ability to form coralloid ectomycorrhizae, which are essentially small compact areas of dense root proliferation that are colonized by the fungus (Molina and Trappe, 1994
). But the scale of the Abies–R. ellenae clumps associated with Sarcodes is far beyond any aggregations that we have observed. In fact, the Sarcodes rootball itself could be viewed as a giant mycorrhiza, one that can be 1000 cm3 or more rather than the typical size of <1 cm3.
If, for the moment, we assume that Abies–R. ellenae clumps develop in response to Sarcodes plants, this creates an apparent mechanistic conundrum. How can a plant that lacks its own carbon source stimulate both its mycorrhizal associate and the roots of the photosynthetic plant to which the fungus is attached? This problem is not as great as it may seem. Growth stimulation of host tissues is a common pattern in parasitic interactions. Generally, abnormal cell enlargement and/or division are mediated by hormonal imbalance associated with infection (Agrios, 1997
). Examples include branch swelling caused by mistletoes, tumors by Agrobacterium, cankers by some rust fungi, and a variety of galls by flies, aphids, and wasps.
Yet these examples differ in at least two ways from the Sarcodes system. First, both R. ellenae, which is directly connected to Sarcodes, and Abies roots, which are not directly connected to Sarcodes, have proliferated. If Sarcodes seeds germinate near pre-existing clumps of R. ellenae ECM, the snow plant could subsequently alter: (a) a R. ellenae mycorrhization pathway that stimulates Abies roots indirectly or (b) an Abies root proliferation pathway that stimulates R. ellenae indirectly. A mechanism for the former process is suggested by indole-3-acetic acid (IAA)-overproducing mutant strains of the ECM fungus Hebeloma cylindrosporum Romagnesi, which can form three to six times more ECM roots with pine hosts than wild-type strains (Durand et al., 1992
; Gay et al., 1994
). A second, and more important difference of the Sarcodes system, is that growth stimulation is likely to benefit R. ellenae. Instead, parasite-induced growth reduces host fitness (e.g., "parasitic castration" of mollusks by trematodes; Sorensen and Minchella, 1998
). In this study, it seems that R. ellenae benefits; it colonizes a vastly larger proportion of Abies roots relative to its competitors in a diverse ECM community. This must in turn benefit the specialized Sarcodes. In this aspect the relationship between Sarcodes and R. ellenae appears mutualistic rather than parasitic.
In summary, we found both fungal and photosynthetic hosts in disproportionate concentrations in rootballs of Sarcodes compared to the adjacent soil. Thus, the ectomycorrhizal community differs significantly where Sarcodes roots are present in a manner that appears beneficial, at least over the short term, to the fungal symbiont. However, we do not know whether there is any trade-off incurred by R. ellenae as a result of its association with Sarcodes. This will be a critical piece of information to acquire if we are to understand the nature of this tripartite symbiosis.
|
|
FOOTNOTES |
|---|
2 Author for correspondence (e-mail: martinb{at}nature.berkeley.edu
).
3 Current address: 2082 Cordley Hall, Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331–2902 USA.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSION LITERATURE CITED |
|---|
Bidartondo, M. I., A. M. Kretzer, and T. D. Bruns. 1998 Identity and spatial distribution of the fungal associate of Sarcodes sanguinea. Inoculum 49: 9
Björkman, E. 1960 Monotropa hypopitys L. an epiparasite on tree roots. Physiologia Plantarum 13: 308–327[CrossRef]
Bruns, T. D., T. M. Szaro, M. Gardes, K. W. Cullings, J. J. Pan, D. L. Taylor, T. R. Horton, A. M. Kretzer, M. Garbelotto, and Y. Li. 1998 A sequence database for the identification of ectomycorrhizal basidiomycetes by phylogenetic analysis. Molecular Ecology 7: 257–272[CrossRef]
Comandini, O., G. Pacioni, and A. C. Rinaldi. 1998 Fungi in ectomycorrhizal associations of silver fir (Abies alba Miller) in central Italy. Mycorrhiza 7: 323–328[CrossRef][ISI]
Cullings, K. W., T. M. Szaro, and T. D. Bruns. 1996 Evolution of extreme specialization within a lineage of ectomycorrhizal epiparasites. Nature 379: 63–66[CrossRef][ISI]
Dahlberg, A., L. Jonsson, and J. E. Nylund. 1997 Species diversity and distribution of biomass above and below ground among ectomycorrhizal fungi in an old-growth Norway spruce forest in south Sweden. Canadian Journal of Botany 75: 1323–1335
Danielson, R. M. 1984 Ectomycorrhizal associations of jack pine in northeastern Alberta. Canadian Journal of Botany 62: 932–939
Duddridge, J. A., and D. J. Read. 1982 An ultrastructural analysis of the development of mycorrhizas in Monotropa hypopitys L. New Phytologist 92: 203–214[CrossRef][ISI]
Durand, N., J. C. Debaud, L. A. Casselton, and G. Gay. 1992 Isolation and preliminary characterization of 5 fluoroindole-resistant and IAA-overproducer mutants of the ectomycorrhizal fungus Hebeloma cylindrosporum Romagnesi. New Phytologist 121: 545–553[CrossRef][ISI]
Francke, H. L. 1934 Beiträge zur Kenntnis der Mykorrhiza von Monotropa hypopitys L. analyse und Synthese der Symbiose. Flora (Jena) 129: 1–52
Furman, T. E., and J. M. Trappe. 1971 Phylogeny and ecology of mycotrophic achlorophyllous angiosperms. Quarterly Review of Biology 46: 219–225[CrossRef]
Gardes, M., and T. D. Bruns. 1993 ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113–118[Medline]
———, and ———. 1996 Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above- and below-ground views. Canadian Journal of Botany 74(10): 1572–1583
Gay, G., L. Normand, R. Marmeisse, B. Sotta, and J. C. Debaud. 1994 Auxin overproducer mutants of Hebeloma cylindrosporum Romagnesi have increased mycorrhizal activity. New Phytologist 128: 645–657[CrossRef][ISI]
Herre, E. A. 1995 Factors affecting the evolution of virulence: nematode parasites of fig wasps as a case study. Parasitology 111: S179-S191[ISI]
Horton, T. R., and T. D. Bruns. 1998 Multiple-host fungi are the most frequent and abundant ectomycorrhizal types in a mixed stand of Douglas fir (Pseudotsuga menziesii) and bishop pine (Pinus muricata). New Phytologist 139: 331–339[CrossRef][ISI]
Jonsson, L., A. Dahlberg, M.-C. Nilsson, O. Zackrisson, and O. Kårén. 1999 Ectomycorrhizal fungal communities in late-successional Swedish boreal forests, and their composition following wildfire. Molecular Ecology 8: 205–215
Leake, J. R. 1994 Tansley Review Number 69: the biology of myco-heterotrophic ("saprophytic") plants. New Phytologist 127: 171–216[CrossRef][ISI]
Miller, S. L., and E. B. Allen. 1992 Mycorrhizae, nutrient translocation, and interactions between plants. In M. F. Allen [ed.], Mycorrhizal functioning: an integrative plant-fungal process. Chapman and Hall, New York, New York, USA
Molina, R., and J. M. Trappe. 1994 Biology of the ectomycorrhizal genus Rhizopogon: I. Host associations, host-specificity and pure culture syntheses. New Phytologist 126: 653–675[CrossRef][ISI]
Natarajan, K., V. Mohan, and K. Ingleby. 1992 Correlation between basidiomata production and ectomycorrhizal formation in Pinus patula plantations. Soil Biology and Biochemistry 24: 279–280[CrossRef]
Price, P. W. 1980 Evolutionary biology of parasites. In R. M. May [ed.], Monographs in population biology. Princeton University Press, Princeton, New Jersey, USA
Robertson, D. C., and J. Robertson. 1982 Ultrastructure of Pterospora andromedea Nuttall and Sarcodes sanguinea Torrey mycorrhizas. New Phytologist 92: 539–551[CrossRef][ISI]
Simard, S. W., R. Molina, J. E. Smith, D. A. Perry, and M. D. Jones. 1997a Shared compatibility of ectomycorrhizae on Pseudotsuga menziesii and Betula papyrifera seedlings grown in mixture in soils from southern British Columbia. Canadian Journal of Forest Research 27: 331–342
———, D. A. Perry, M. D. Jones, D. D. Myrold, D. M. Durall, and R. Molina. 1997b Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 338: 579–582[CrossRef]
Smith, S. E., and D. J. Read. 1997 Mycorrhizal symbiosis, 2nd ed. Academic Press, San Diego, California, USA
Sorensen, R., and D. J. Minchella. 1998 Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails. Oecologia 115: 188–195[CrossRef][ISI]
Stendell, E., T. R. Horton, and T. D. Bruns. 1999 Early effects of prescribed fire on the structure of the ectomycorrhizal fungal community in a Sierra Nevada ponderosa pine forest. Mycological Research 103: 1353–1359[CrossRef][ISI]
Swofford, D. L. 1993 PAUP: phylogenetic analysis using parsimony, version 3.1.1. Illinois Natural History Survey, Champaign, Illinois, USA
Taylor, D. L., and T. D. Bruns. 1997 Independent, specialized invasions of ectomycorrhizal mutualism by two non-photosynthetic orchids. Proceedings of the National Academy of Sciences (USA) 94: 4510–4515[CrossRef]
Thompson, J. N. 1994 The coevolutionary process. University of Chicago Press, Chicago, IL
Vreeland, P., E. F. Kleiner, and H. Vreeland. 1981 Mycorrhizal symbiosis of Sarcodes sanguinea. Environmental and Experimental Botany 21: 15–25
Wallace, G. D. 1975 Studies of the Monotropoideae (Ericaceae): taxonomy and distribution. Wasmann Journal of Biology 33: 1–88
White, T. J., T. D. Bruns, S. Lee, and J. W. Taylor. 1990 Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White [eds.], PCR protocols: a guide to methods and applications. Academic Press, San Diego, California, USA
This article has been cited by other articles:
|
|
 |
|
  H. A. Violi, J. A. Menge, and R. J. Beaver Chaetomium elatum (Kunze: Chaetomiaceae) as a root-colonizing fungus in avocado: is it a mutualist, cheater, commensalistic associate, or pathogen? Am. J. Botany, April 1, 2007; 94(4): 690 - 700. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Kjoller and T. D. Bruns Rhizopogon spore bank communities within and among California pine forests Mycologia, July 1, 2003; 95(4): 603 - 613. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. D. Bruns, M. I. Bidartondo, and D. L. Taylor Host Specificity in Ectomycorrhizal Communities: What Do the Exceptions Tell Us? Integr. Comp. Biol., April 1, 2002; 42(2): 352 - 359. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
