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Universität Tübingen, Lehrstuhl Spezielle Botanik und Mykologie, Auf der Morgenstelle 1, D-72076, Tübingen, Germany
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ABSTRACT |
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Cellular interaction of the basidiomycete Tuberculina persicina with the haploid stages of two rusts Puccinia silvatica and Tranzschelia pruni-spinosae was analyzed by serial-section electron microscopy of chemically fixed samples and samples subjected to high-pressure freezing and freeze substitution. Tuberculina persicina is a contact parasite, forming neither haustoria nor other intracellular structures. However, at contact areas between T. persicina and its hosts, distinct interfungal interactions are present. At the beginning, a hyphal cell of T. persicina invades the host cell wall with a protuberance and the cell walls of both protuberance and host cell dissolve at the point of contact. Thus, the plasma membranes of the two organisms contact and fuse to form a pore that enlarges to a final diameter of approximately 1 µm. The membrane of the fusion pore is continuous with the plasma membranes of both cells, and Tuberculina nuclei and other organelles are transferred to the rust cells. Phylogenetic and functional aspects of this curious basidiomycetous interfungal interaction are discussed, and a hypothesis of the evolutionary derivation of the Tuberculina mycoparasitism from a sexual interaction is presented.
Key words: high-pressure freezing, mycoparasitism, rusts, sexuality, Tuberculina, ultrastructure, Urediniomycetes
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Swann and Taylor 1993). Mycoparasites occur in two of these groups; while scattered throughout the Urediniomycetes, mycoparasites form one of the basal lineages of the Hymenomycetes, the Tremellales sensu Bandoni (1984) (Swann et al 2001, Weiß and Oberwinkler 2001). Urediniomycetous mycoparasites include the genera Colacogloea, Colacosiphon, Cryptomycocolax, Cystobasidium, Heterogastridium, Mycogloea, Naohidea, Occultifur, Spiculogloea, Zygogloea and some species of Platygloea (Bandoni 1956, 1984, Kirschner et al 2001, Oberwinkler 1990, Oberwinkler and Bauer 1990, Oberwinkler et al 1990a, b, Roberts 1994, 1996, 1997). However, the phenomenon of mycoparasitism might be more widespread among Urediniomycetes than currently is suspected. One of the recent examples in this respect is the hyphomycetous genus Tuberculina. Tuberculina species are distributed all over the world, living in association with more than 150 rust species from at least 15 genera. Yet, the association between plants, rusts and Tuberculina has been controversial; Tuberculina species were interpreted as mycoparasites specific to rusts (Tubeuf 1901, Zambettakis et al 1985), as nonspecific parasites on several substrates (Petrak 1956, Schroeter 1889), or even as specialized parasites on rust-infected plant tissues, suppressing the rusts by enzymatically destroying their nutrient source (Hulea 1939, Wicker 1981, Wicker and Woo 1969, 1973).
We recently have shown (i) that Tuberculina species are mycoparasites of the haploid stages of rusts, interacting with their hosts via large fusion pores and (ii) that Tuberculina species are members of the Urediniomycetes being closely related to their hosts (Lutz et al 2003). Here, we describe in detail the cellular interaction of Tuberculina persicina with the haploid stages of two rusts Puccinia silvatica and Tranzschelia pruni-spinosae.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Conventional chemical fixation. – Samples were fixed with 2% glutaraldehyde in 0.1 M sodium cacodylate buffer (pH 7.2) at room temperature overnight. After six transfers in 0.1 M sodium cacodylate buffer, samples were postfixed in 1% osmium tetroxide in the same buffer for 1 h in the dark, washed in distilled water and stained in 1% aqueous uranyl acetate for 1 h in the dark. After five washes in distilled water, samples were dehydrated in acetone with 10 min changes at 25, 50, 70, 95%, and three times in 100% acetone. Samples were embedded in Spurr’s plastic and sectioned with a diamond knife. Ultrathin serial sections were mounted on formvar-coated, single-slot copper grids, stained with lead citrate at room temperature for 5 min and washed with distilled water. They were examined with a transmission electron microscope operating at 80 kV.
High-pressure freezing and freeze substitution. –
Infected areas of leaves were removed with a 2 mm cork borer. To remove air from intercellular spaces, samples were infiltrated with distilled water containing 6% (v/v) (2.5 M) methanol for approximately 5 min at room temperature. Single samples were placed in an aluminium holder (one half with a hollow of 0.3 mm depth for the sample and the other a flat top) and frozen immediately in the high-pressure freezer HPM 010 (Balzers Union, Lichtenstein) as described in detail by Mendgen et al (1991). Substitution medium (1.5 ml per specimen) consisted of 2% osmium tetroxide in acetone, which was dried over calcium chloride. Freeze substitution was performed at –90, –60 and –30 C, 8 h for each step, using a Balzers’ freeze substitution apparatus FSU 010. The temperature then was raised to approximately 0 C over 30 min and samples were washed in dry acetone for another 30 min. Infiltration with an Epon/Araldite mixture (Welter et al 1988) was performed stepwise: 30% resin in acetone at 4 C for 7 h, 70 and 100% resin at 8 C for 20 h each and 100% resin at 18 C for approximately 12 h. Samples then were transferred to fresh medium and polymerized at 60 C for 10 h. Finally, samples were processed as described above for chemically fixed samples, except that the sections were stained with 1% aqueous uranyl acetate for 1 h.
Number of investigated interaction sites. – From both the interaction between Tuberculina persicina and Tranzschelia pruni-spinosae and between T. persicina and Puccinia sylvatica, more than 50 high-pressure frozen interaction sites and more than 50 chemically fixed interaction sites were investigated and photographed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, 9–12 and FIGS. 3–8, respectively. By both fixation techniques, the general interaction architecture was recognizable. In high-pressure frozen samples, however, interaction morphology had a more regular appearance and was more distinct than after conventional fixation (cf. FIGS. 1, 2 and FIGS. 3, 4). In addition, membranes were generally smoother after freeze substitution than after conventional fixation. Thus, in high-pressure frozen samples, the plasma membrane followed the contour of the cell wall closely, whereas in conventionally fixed samples, the plasma membrane often was folded irregularly.
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). Hyphae of both Tuberculina and the rusts were clampless but could be distinguished from each other by the number of nuclei per hyphal cell, the diameter of the nuclei and the thickness of the cells walls (FIGS. 1, 3, 5, 7). Hyphae of Tuberculina generally were multinucleate; whereas those of the two rusts usually were mononucleate (bi-nucleate rust hyphal cells occurred only at the base of the aecia). Diameter of the nuclei (on average 1.5 µm in Tuberculina persicina, 3.5 µm in Puccinia sylvatica and 4.5 µm in Tranzschelia pruni-spinosae) and thickness of the cell walls (on average 0.08 µm in T. persicina, and 0.22 in T. pruni-spinosae and P. sylvatica) of the two rusts were roughly more than twice as large as those of Tuberculina (FIGS. 1, 3, 5, 7). Interaction stages between Tuberculina and the two rusts frequently were found in neighboring areas of the aecia, especially at the base of them. In these interaction, the protoplasts of both—the Tuberculina and the rust hyphal cells—were fused via a large pore of approximately 1 µm diam (FIGS. 1–8). Especially in high-pressure frozen interaction sites, the membrane of the fusion pore clearly was observed to be continuous with the plasma membranes of both the Tuberculina and the rust cell (FIG. 6). Transfer of nuclei and other organelles from Tuberculina cells through the fusion pores into rust cells was evident. Thus, mitochondria (FIG. 8) and Tuberculina nuclei (FIGS. 3, 4, 5) were observed extending through the fusion pores into the rust cells. In addition, interaction stages were observed in which Tuberculina nuclei were located within the rust cells close to rust nuclei (FIGS. 7, 8). A reverse transfer from rust cells to Tuberculina cells, however, was not observed.
Development. –
Although it is not possible from electron micrographs to determine directly the development, the comparison of many and especially different developmental stages permits their arrangement in a logical and plausible series. By doing so, the cellular interaction between Tuberculina persicina and the two rusts Tranzschelia pruni-spinosae and Puccinia silvatica revealed this pattern of events: In the initial stages of interaction, a hyphal cell of Tuberculina in contact with that of the rusts invades the rust cell wall with a protuberance (FIG. 9). The Tuberculina cell wall surrounding the protuberance apparently dissolves (FIG. 9), and during its penetration of the host cell wall the host cell wall adjacent to the protuberance gradually dissolves (FIGS. 9–12). The protuberance subsequently enlarges (FIGS. 10–12), and the plasma membranes of the two organisms contact each other (FIG. 12) and fuse to form a pore between them. The fusion pore then enlarges to a final diameter of approximately 1 µm (FIGS. 1–4, 5, 7, 8). This process also is reflected by interpreting serial sections of one interaction stage, beginning from the margin of the interaction to the center (partly illustrated in FIGS. 10–12).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, b, 1991, 2003, Kirschner et al 2001, Oberwinkler and Bauer 1990, Oberwinkler et al 1990a, c, 1999, Zugmaier et al 1994). From these data, the basidiomycetous interfungal cellular interactions can be divided into two main types at the structural level.
One type is the colacosome-interaction. Mycoparasites in the Microbotryomycetidae (Bauer et al 1997, Swann et al 1999) generally are characterized by their interaction via a unique organelle, the colacosome, formed in abundance at the interface between the parasite and its fungal host (Bauer and Oberwinkler 1991, 2003, Kirschner et al 2001, Oberwinkler and Bauer 1990, Oberwinkler et al 1990a, 1999). This mycoparasitic organelle first was described in detail from the interaction of the parasite Colacogloea peniophorae (Bourd. & Galz.) Oberw. & Bandoni and its host, Hyphoderma praetermissum (Karst.) Erikss. & Strid. (Bauer and Oberwinkler 1991, Oberwinkler et al 1990a). During the interaction, the membrane-bound core of the colacosomes intrudes into the host cell wall. Thus, colacosomes combine the hyphal cells of the parasite with those of the host fungus, serving as connecting agents. Accordingly, the formation of colacosomes results in a greatly increased contact zone between the parasite and its host (Bauer and Oberwinkler 1991). An additional type of colacosome was found in Cryptomycocolax (Oberwinkler and Bauer 1990). Colacosomes of this type are capable of fusing with the host cell via a small pore of 7–14 nm diam. The fusion-interaction reported here for Tuberculina is not of the colacosometype. Colacosomes are not developed by Tuberculina. In addition, in contrast with the Tuberculina interaction, in Cryptomycocolax the colacosomes fuse only with the host cells but not the parasitic cytoplasm as in Tuberculina.
The other basidiomycetous mycoparasitic interaction type is the fusion-interaction. Typical fusion mycoparasites (Bauer and Oberwinkler 1990a, b, Zugmaier et al 1994) are the Tremellales (including the Filobasidiales) of the Hymenomycetes (Bandoni 1984, 1995). However, fusion mycoparasites also are scattered throughout the Urediniomycetes. For example, the members of Cystobasidium, Mycogloea, Naohidea, Occultifur, Spiculogloea and Zygogloea are fusion mycoparasites (unpublished data). Basidio-mycetous fusion mycoparasites usually interact with their respective hosts by specialized interactive cells often designated as "tremelloid haustorial cells". These cells first were described and designated as "haustoria" by Olive (1947). Each tremelloid haustorial cell is subtended by a clamp and consists of a subglobose basal part with one or more thread-like filaments (e.g., Oberwinkler et al 1984) that are capable of fusing with host cells via a small pore 14–19 nm diam (Bauer and Oberwinkler 1990a, 1990b, Zugmaier et al 1994). Thus, in these mycoparasites as in the Tuberculina interaction, a direct cytoplasm-cytoplasm connection between the parasites and their respective hosts occurs. However, the Tuberculina interaction differs significantly from the known basidiomycetous fusion-interactions in the lack of specialized interactive cells and particularly in the diameter of the fusion pore of approximately 1 µm and in the transfer of Tuberculina nuclei into the rust cells. These characteristics make the Tuberculina interaction unique among the basidiomycetous inter-fungal fusion interactions.
Functional aspects. –
Direct cytoplasm-cytoplasm connections between mycoparasites and their respective hosts represent an unusual type of cellular interaction. This type of interaction may be efficient because substances required by the parasite do not cross membranes or cell walls. Thus, the fusion pores serve as direct avenues for nutrients (Hoch 1977). In this respect, however, the Tuberculina interfungal interaction is fundamentally different from those of the other basidiomycetous fusion parasites. In contrast with the Tuberculina interaction, the small fusion channels of the plasmodesmata in the other basidiomycetous fusion interactions prevent the exchange of organelles between the interacting organisms and the uncontrolled transport of substances from cell to cell (Bauer and Oberwinkler 1990a). On the other hand, the large opening between Tuberculina and its hosts permits free cytoplasmic exchange between the interacting organisms with transfer of organelles. In fact, in the Tuberculina interaction, nuclei and other organelles are transferred to the rust cells. As an immediate consequence of this fusion event, nuclei of both partners come into close contact. This scenario suggests compatibility between the genomes of the interacting organisms that prevents elicitation of rejection responses ( Jeffries and Young 1994), but the obvious questions to address are: Which effects are caused by the transferred Tuberculina nuclei? Does this intimate interspecific nuclear contact lead to a parasexual recombination event with transfer of genetic information, as it is described from the zygomycetous Parasitella-Absidia system (Kellner et al 1993)? After infection the fate of the two interacting organisms is completely different. Thus, the development of Tuberculina continues with the formation of sporodochia, whereas the development of the host rust stops or becomes at least significantly slowed after infection.
Hypothesis for the evolutionary origin of the Tuberculina mycoparasitism. –
Tuberculina species are haploid and are closely related to their hosts, the rusts. Thus, Tuberculina species as well as rusts are members of the Urediniomycetidae (Lutz et al 2003). Except for Tuberculina, mycoparasitism is unknown in this group. In addition, the closest relatives of Tuberculina, such as the rusts, Iola, Eocronartium and Herpobasidium, are plant parasites (Bauer and Oberwinkler 1994, Oberwinkler and Bandoni 1984). From this situation the question arises: How could an ancestor in this group evolve the power to parasitize rust fungi and to establish a fusion interaction permitting the transfer of organelles? Tuberculina, it is astonishing to note, parasitizes only the haploid stages of rusts (Lutz et al 2003), and within the Urediniomycetidae and the Basidiomycota only Tuberculina and the rusts have distinct fructifications in the haploid phase. In fact, Tuberculina sporodochia (Ditmar 1817, Lutz et al 2003) resemble rust pycnia of type 2 (Hiratsuka and Hiratsuka 1980) in also having subepidermal, determinate and flat hymenia without bounding structures and sterile elements. Of interest, type 2 was interpreted by Hiratsuka and Hiratsuka (1980) as the simplest type of rust pycnia, occurring in the genera Hyalopsora, Chrysomyxa, Melampsora, Uredinopsis and Coleosporium. In addition, the parasitic Tuberculina interaction scenario closely resembles intraspecific fusion events occurring during formation of hyphal anastomoses and during entry into sexual reproduction (e.g., Aylmore and Todd 1984, Hawker and Beckett 1971, Melkonian 1980, Newhouse and MacDonald 1991). Furthermore, a similar parasitic fusion-interaction scenario with horizontal nuclear transfer between closely related organisms is known (i) from the zygomycetous Parasitella-Absidia system, in which the parasitic interaction is mediated by the sex pheromone trisporic acid and in which an evolutionary link between parasitism and sexuality has been proposed (Burgeff 1924, Wöstemeyer et al 1995), and (ii) from some adelphoparasites of red algae, in which the development and physiology of the parasites are similar to normal post-fertilization processes in the hosts (Goff and Zuccarello 1994) and from which a direct evolution of the parasites from their respective hosts has been postulated (Goff et al 1996). Does the Tuberculina mycoparasitism, as postulated in these examples, also have a sexual basis, deriving from a modified mating interaction, and accordingly do Tuberculina and the rust pycnia have a direct common evolutionary origin? This hypothesis at least would explain the phenomenon that Tuberculina parasitizes only the haploid stages of rusts (Lutz et al 2003), but additional studies on this fascinating system concerning the morphology of Tuberculina sporodochia and rust pycnia, the precise rust-Tuberculina phylogenetic relationship and the genetic background of the Tuberculina parasitism are needed to clarify this hypothesis.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Part 214 in the Series "Studies in Heterobasidiomycetes" from the Botanical Institute, University of Tübingen. 
2 Corresponding author. E-mail: robert.bauer{at}uni-tuebingen.de
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