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Universität Tübingen, Botanisches Institut, Lehrstuhl Spezielle Botanik und Mykologie, Auf der Morgenstelle 1, D-72076 Tübingen, Germany
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Tuberculina species are mitosporic parasites of rust fungi. It was demonstrated recently that Tuberculina represents the asexual life stage of the plant-parasitic genus Helicobasidium. Here we reveal the host specificities of Tuberculina and Helicobasidium species on rust fungal hosts by means of infection experiments and molecular analyses. We inoculated species of the rust genera Chrysomyxa, Coleosporium, Cronartium, Gymnosporangium, Puccinia, Tranzschelia and Uromyces with conidia and with basidiospores of Helicobasidium longisporum and H. purpureum and with conidia of Tuberculina maxima, T. persicina and T. sbrozzii. In addition we analyzed base sequences from the nuclear ITS region of 51 Tuberculina and Helicobasidium specimens collected in the field together with the sequences from the Tuberculina infections obtained by infection experiments. The resulting data show that at least six monophyletic lineages are within the Tuberculina/Helicobasidium-group that can be unambiguously distinguished by combining molecular and morphological characters and by specific host spectra of the Tuberculina-stage. This diversity opens up new vistas on the evolution of this exceptional mycoparasitic-phytoparasitic fungal group.
Key words: Helicobasidium, host specificity, infection experiments, ITS, Tuberculina, molecular phylogeny, mycoparasitism, Urediniomycetes
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, b). In contrast to the mycoparasitic genus Tuberculina, Helicobasidium species are serious plant pathogens causing the economically important violet root rot. They are unspecific in their choice of hosts (Buddin and Wakefield 1924, Hering 1962) and reported as parasites of more than 120 plant species representing more than 50 families of the spermatophytes and ferns (Itô 1949, Viennot-Bourgin 1949). Extensive research has been conducted on the biology of and the combat against Helicobasidium, but the diversity of the genus remains poorly understood (Aimi et al 2003a, b; Uetake et al 2002) and hypotheses on the life cycle conflict (Aimi et al 2003b, Lutz et al 2004a).
Although the strong inhibitory effect of Tuberculina on rust spore production has resulted in extensive research dealing with Tuberculina as an agent in biological rust control (for review see Wicker 1981), the relationship among Tuberculina, rusts and plants was the subject of controversy. Tuberculina species have been interpreted as mycoparasites specific to rusts (Kirulis 1940, Tubeuf 1901, Tulasne 1854, Zambettakis et al 1985), as nonspecific parasites on several substrates (Petrak 1956, Schroeter 1889) or even as specialized parasites on rust-infected plant tissues (Biraghi 1940; Hulea 1939; Marchal 1902; Wicker and Woo 1969, 1973). Thus plant parasites and parasites of non-rust fungi were included in the genus adopting a concept based on morphological characters (Ellis 1893, Patouillard and Gaillard 1888). Other authors used a species concept based on host specificities, distinguishing Tuberculina species on different rust hosts (Spegazzini 1880, 1884) or even plant hosts (Gobi 1885). However, Barkai-Golan (1959) demonstrated that Tuberculina could not infect rust-free plants and we recently substantiated the mycoparasitic nature of Tuberculina persicina on rust fungal hosts by ultrastructural observations that reveal a specific and morphologically uncommon cellular interaction via large fusion pores with a direct cytoplasm-cytoplasm connection and interspecific transfer of Tuberculina-nuclei to rust hyphae (Bauer et al 2004, Lutz et al 2004b).
Even though several authors described Tuberculina species based on the occurrence on different hosts (e.g., Spegazzini 1880, 1884) and the vast majority of Tuberculina maxima specimens are described from Cronartium- and Gymnosporangium- hosts, no experimental proof for host specificity of any Tuberculina species was provided. On the contrary, Barkai-Golan (1959) demonstrated that Tuberculina persicina specimens from one rust host are capable of infecting several other rust species.
In this report, we present both results of infection experiments and molecular data that reveal the host specificities of several Tuberculina and Helicobasidium lineages, respectively, on their rust fungal hosts. These findings yield new insights in the Tuberculina–Helicobasidium life cycle and in the diversity of the group.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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We have gathered data on inoculated rust species, the species used as inocula, the results of the different inoculations, the respective kind of inoculum and the respective experimental approach of the different inoculations (TABLE I).
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We used two kinds of inocula: (i) We collected intensively sporulating basidiocarps of Helicobasidium longisporum and H. purpureum in the field, tore the fresh basidiocarps into pieces of about 4 square cm and tagged the pieces to pear trees at the same places where we had fixed the rust inocula before (cf. below); (ii) basidiospores from freshly collected basidiocarps (pieces of about 4 cm2 were used) or conidia were shaken vigorously by hand in tap water (75 mL). The conidia were either from freshly collected Tuberculina sporodochia or from sporodochia that were conserved at –18 C in a freezer (cf. Wicker and Wells 1968) (in both cases we used about 20 sporodochia) or from Tuberculina or Helicobasidium cultures (about 3 g of fungal material were used). The inoculum was spread over the top and the underside of rust-infected leaves with a brush. In every case we inoculated the rusts with their hyperparasites as soon as the rust spermogonia were mature.
The rusts for inoculation were obtained in four different ways. Accordingly, four experimental settings were established. (i) Rust-infected plants growing in nature were used (Chrysomyxa rhododendri on Picea abies, Coleosporium tussilaginis on Pinus sylvestris, Cronartium ribicola on Pinus aristata, Gymnosporangium cornutum on Sorbus aucuparia, Puccinia sessilis on Allium ursinum, and Tranzschelia prunispinosae on Anemone ranunculoides). We chose places where we were not able to detect any Tuberculina infection in the previous growth season. We divided the places in isolated areas where we inoculated the rust infected plants and areas without inoculation for control. (ii) We inoculated pear trees growing in nature with Gymnosporangium sabinae to obtain heavy rust infections. To this end we attached freshly collected branches of Juniperus sp., which showed intensive infections with germinating and sporulating teliospores of Gymnosporangium sabinae to several distant trees where we were not able to detect any Tuberculina infection in the previous vegetation period. One rust-inoculated, isolated tree at each location served as control and was not inoculated with the hyperparasite. (iii) We transferred Euphorbia cyparissias plants that systemically were infected by Uromyces pisi s.l., young shoots of Vinca major infected with Puccinia vincae and little Pinus sylvestris trees infected with Coleosporium tussilaginis from nature to our greenhouse. The plants inoculated with the hyperparasite and control plants were cultivated in different houses. After inoculation the single plants were incubated 3 d under transparent plastic bags to provide high relative humidity. (iv) We cultivated Taraxacum officinale agg. in our greenhouse and infected the plants with Puccinia silvatica using the wire net method (Kakishima et al 1999). Freshly collected leaves of Carex brizoides L. harboring sori of teliospores of the rust, which were incubated at room temperature 3 d in plastic bags at high humidity, served as inoculum. Inoculation with the hyperparasite and control were handled as in (iii).
Inoculated plants and the control then were observed until the respective rusts completed their life cycles on the respective host plant. If sporodochia were detected, the Tuberculina infection was verified microscopically and a part of the material was conserved for further examinations.
Field observations. –
We checked several rust species growing in an area of 200 square m around several sporulating basidiocarps of Helicobasidium purpureum for Tuberculina infections during 2 y, and we introduced some additional plant species harboring young spermogonia of different rust species at that place (TABLE II).
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Molecular analyses. –
We isolated genomic DNA from 41 herbarium specimens and from four cultures on artificial media of Tuberculina and Helicobasidium, respectively (TABLE III). We followed the methods of isolation and crushing of fungal material, DNA extraction, amplification, purification of PCR products, sequencing and processing of raw data of Lutz et al (2004b). To ensure that the observed Tuberculina infections could be ascribed to the respective inocula and to infer the phylogeny of the sampled Tuberculina and Helicobasidium specimens, we amplified the ITS1/2 region of the rDNA including the 5.8S rDNA (ITS, about 600 bp) using the primer pair ITS1 and ITS4 (White et al 1990). For amplification of the ITS region we adjusted the annealing temperature to 45 C. DNA sequences determined for this study were deposited in GenBank (TABLE III).
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DNA sequences were aligned under default settings with Clustal X (Thompson et al 1997). The alignment subsequently was improved with Rascal (Thompson et al 2003). We did not manipulate the alignment by hand or excluded any positions as recommended by Giribet and Wheeler (1999) and Gatesy et al (1993), respectively. The final alignment (75 sequences; length 598 bp, 103 variable sites) and the published tree are deposited in TreeBase (http:// treebase.bio.buffalo.edu/treebase/) with the study accession number S1061 and the matrix accession number M1811. Sequence distances were computed with the MEGALIGN module of the Lasergene package (DNASTAR Inc., Madison, Wisconsin).
To estimate phylogenetic relationships we used a Bayesian approach of phylogenetic inference using a Markov Chain Monte Carlo (MCMC) technique as implemented in the computer program MrBayes 3.0b4 (Huelsenbeck and Ronquist 2001). For Bayesian analysis, the data first were analyzed with MrModeltest 1.0b ( J.A.A. Nylander, Upsala University, Sweden; Posada and Crandall 1998) to find the most appropriate model of DNA substitution. The hierarchical likelihood ratio test proposed the DNA substitution model of Hasegawa, Kishino and Yano (HKY, Hasegawa et al 1985) with gamma distributed substitution rates (see Swofford et al 1996). Thus, four incrementally heated simultaneous Markov chains were run over 2 000 000 generations using the HKY model of DNA substitution with gamma distributed substitution rates, random starting trees and default starting parameters of the DNA substitution model. Trees were sampled every 100 generations, resulting in an overall sampling of 20 001 trees. From these, the first 1001 trees were discarded (burn in = 1001). The trees (19 000)* remained static and were used to compute a 50% majority rule consensus tree to obtain estimates for the a posteriori probabilities of groups of species. This Bayesian approach of phylogenetic analysis was repeated 10 times to test the independence of the results from topological priors (cf. Huelsenbeck et al 2002).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Infections of rust aecia were observed for inoculations with both Tuberculina and Helicobasidium. No differences were found among inoculations with basidiospores, conidia from Tuberculina sporodochia or conidia from Tuberculina and from Helicobasidium cultures. Sporodochia were observed 2–6 wk after inoculation in 20–50% of the rust aecia and rapidly increased to include up to 95% of the aecia by the end of the aecial phase of the rust life cycle. Tuberculina infections never were observed in the control experiments. The actual derivation of the infections from the inocula was approved by the distribution of the infections being localized at the places of inoculation and by analyzing ITS base sequences of inoculum and infection with Tuberculina infections showing identical base sequences compared to the respective inocula (cf. below). For other inoculations, infections never were observed.
Field observations. –
We have provided results of our 2 y observation of the rust flora, including some experimentally introduced rust species, around Helicobasidium purpureum basidiocarps (TABLE II).
Infection pattern. –
Analyzing the pattern of infection and noninfection of the sampled rust species, the differences in the susceptibility of different rust hosts with respect to Helicobasidium and Tuberculina species and even to specimens of Tuberculina persicina became obvious. Tuberculina obtained from Helicobasidium purpureum infections were restricted to Puccinia spp., Tranzschelia prunispinosae and Uromyces pisi s.l., and in either case the inoculations resulted in Tuberculina persicina infections. Tuberculina persicina conidia from sporodochia on Puccinia silvatica could infect only Puccinia silvatica and Uromyces pisi s.l. For both inocula, we never obtained infections of Chrysomyxa, Coleosporium, Cronartium and Gymnosporangium species. The field observation is of the same tenor. Tuberculina persicina infections presumably caused by Helicobasidium purpureum basidiospores never were observed on Coleosporium and Gymnosporangium species but on several other rusts, whereat the host spectrum is extended to Melampsora, Ochropsora and other Puccinia, Tranzschelia and Uromyces species (TABLE II). In contrast, Helicobasidium longisporum caused only Tuberculina persicina infections of Gymnosporangium spp. and Tuberculina persicina conidia from sporodochia on Gymnosporangium sabinae were successful only on Gymnosporangium spp. For both inocula, we never obtained infections of Chrysomyxa, Coleosporium, Cronartium, Puccinia, Tranzschelia and Uromyces species. Tuberculina maxima conidia from sporodochia on Gymnosporangium sabinae were successful only on the original host Gymnosporangium sabinae, never on Chrysomyxa, Coleosporium, Cronartium, Puccinia, Tranzschelia and Uromyces species. Puccinia vincae was susceptible only to Tuberculina sbrozzii conidia from sporodochia, which were collected on the same host, and not to Tuberculina maxima, T. persicina, Helicobasidium longisporum and H. purpureum.
Molecular analyses. – The first aim of molecular analyses was to test whether the Tuberculina infections obtained in the infection experiments actually originated from the respective inocula. In fact we observed identical ITS base sequences for Helicobasidium purpureum (AY254189 [GenBank] , AY460132 [GenBank] ) and Tuberculina persicina inocula (AY460169 [GenBank] ) and the respective T. persicina infections (AY254190 [GenBank] , AY254191 [GenBank] , AY254192 [GenBank] , AY254193 [GenBank] , AY460167 [GenBank] , AY460168 [GenBank] , AY460174 [GenBank] , AY460175 [GenBank] ), H. longisporum (AY254187 [GenBank] , AY254188 [GenBank] ) and T. persicina inocula (AY460155 [GenBank] ) and the respective T. persicina infections (AY254194 [GenBank] , AY254195 [GenBank] , AY460152 [GenBank] , AY460153 [GenBank] ), T. maxima inoculum (AY460141 [GenBank] ) and the respective infection (AY460138 [GenBank] ), and T. sbrozzii inoculum (AY460171 [GenBank] ) and the respective infection (AY460172 [GenBank] ).
Furthermore, we inferred the phylogenetic relationships of the specimens used in the infection experiments together with specimens collected in the field and sequences from GenBank that cover most of the hitherto known diversity of the Helicobasidium/Tuberculina-group. The Bayesian phylogenetic analyses yielded consistent topologies. We present the consensus tree of one run to illustrate the results (FIG. 1). The topology is consistent with recent analyses of ITS (Uetake et al 2002), LSU (Lutz et al 2004b) and combined ITS/LSU (Lutz et al 2004a) sequence datasets, but more taxa are included and it provides higher resolution. The phylogenetic hypothesis reveals two major groups with considerable genetic distance. The first consists of Helicobasidium mompa and the sister taxa H. longisporum I and H. longisporum II (each with the mitosporic life stage Tuberculina persicina). The second group comprises two clusters of T. maxima, one composed of specimens with Gymnosporangium sabinae-hosts (designated as T. maxima II), the other with Cronartium-hosts (designated as T. maxima I), and a group of H. purpureum, T. persicina and T. sbrozzii specimens. While the a posteriori probabilities for the branching in the H. mompa/H. longisporum-group are ideal, the Tuberculina maxima II-group lacks any support and the sister-group relationship of the highly supported H. purpureum-group (a posteriori probability 100%) and of the moderately supported Tuberculina maxima I-group (87%) is supported only weakly (75%). Within the H. purpureum-cluster, all specimens of T. sbrozzii fall into one clade.
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). In addition, including the sequences from GenBank and the specimens collected in the field, the phylogenetic analysis reveals that the groups within Helicobasidium/Tuberculina, as far as tested in the infection experiments, refer to the pattern of infection and noninfection of rust hosts. The only exception is the H. longisporum II-group with its T. persicina-stage on Puccinia sp. and Crossopsora notata.
All Tuberculina specimens collected in the field observation area around H. purpureum basidiocarps cluster in the H. purpureum-group (cf. black stars in FIG. 1). In contrast to the infection experiments, two sequences of Tuberculina specimens collected in the field observation area (AY460165
[GenBank]
, AY460170
[GenBank]
) show a divergence of 0.5% compared to that of the presumable inoculum (Helicobasidium purpureum AY254189
[GenBank]
) and compared to those of the other observed infections and a divergence of 0.4% compared to each other.
It is of interest to note that ITS sequences from specimens collected at distant places are identical in the groups H. mompa (the sampled sequences just represent many others from GenBank, which are identical), H. longisporum I, T. maxima II, and T. sbrozzii. In contrast, sequence variability ranges from identity to 1.3% divergence in H. purpureum and from identity to 0.7% divergence in H. longisporum II. In T. maxima I the specimens from North America (AY292435 [GenBank] , AY292436 [GenBank] , AY292437 [GenBank] , AY460136 [GenBank] ) possess identical ITS sequences and show 1.3% divergence compared to the European specimen (AY460135 [GenBank] ).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). That lineages seem to be restricted to host species of one rust genus (Tuberculina maxima I, T. maxima II, Helicobasidium longisporum I) or even to few closely related species (Tuberculina sbrozzii) was of interest to us. In contrast the Tuberculina-stage of Helicobasidium purpureum is capable of parasitizing species of several rust genera (Endophyllum, Kuehneola, Melampsora, Ochropsora, Phragmidium, Puccinia, Tranzschelia and Uromyces), which represent diverse phylogenetic lineages of the rusts (for rust phylogeny see Maier et al 2003). Two members of the rust family Coleosporiaceae (the type genus Coleosporium and Chrysomyxa) conversely were not susceptible at all to Tuberculina, and despite intensive collection no Tuberculina infections of those genera have been reported. In contrast, Gymnosporangium species are susceptible for both Tuberculina maxima II and the Tuberculina-stage of Helicobasidium longisporum I. The observed host specificities of the Tuberculina-stage are in contrast to the unspecific choice of plant hosts of the Helicobasidium-stage (Duggar 1915, Hering 1962, Itô 1949, Viennot-Bourgin 1949).
The combination of host specificities, morphological and molecular characters reveals more lineages within the Tuberculina/Helicobasidium-group than hitherto distinguished (in the case of Tuberculina see Ellis and Ellis 1988; for Helicobasidium see Roberts 1999, Uetake et al 2002) and consequently demands a revision of the species concept within the group to cope adequately with the diversity. The genus Tuberculina should be restricted to rust parasites, and species delimitation requires both morphological and molecular characters, as well as information about the host spectrum. Taxonomical conclusions are in preparation.
Diversity and evolution of the Tuberculina/Helicobasidium-group. –
Synopsis of host specificities, ecology, morphological and molecular characters reveals these seven groups (cf. FIG. 1):
). Unfortunately, no Tuberculina specimens from Asia were available. Helicobasidium mompa was demonstrated to have a uniform population structure, presumably reproducing mainly or exclusively asexually via hyphae or sclerotia (Katsumata et al 1996). The clonal population structure is suggested by the uniformity of ITS sequences of Helicobasidium mompa isolates. Uetake et al (2002) showed that among 17 isolates from several host plants in Japan and Korea only two had a single base substitution. Consequently, one could think of a species that is adapted to the life in annually disturbed habitats (cf. Uetake et al 2003) and that possibly is not dependent on the Tuberculina-stage for reproduction. , data corresponding to our observations) and by its small-spored Tuberculina-stage, which seems to be restricted to Gymnosporangium species. Even though both the Helicobasidium-and the Tuberculina-stage are present and, as a consequence sexual reproduction could be assumed, the specimens collected in Greece (AY292443
[GenBank]
[GenBank]
), Austria (AY292444
[GenBank]
[GenBank]
) and Germany (AY254187
[GenBank]
[GenBank]
, AY460154
[GenBank]
[GenBank]
) show identical ITS base sequences. ). ) but is restricted to Cronartium- hosts. We found it interesting to note that the specimens from North America clearly are separated by the molecular data from the European specimen. This supports the indigenous nature of that lineage that was assumed by Mielke (1933), considering the distribution of T. maxima on several Cronartium species. , data corresponding to our observations). The species’ Tuberculina-stage is small-spored (7–10 µm diam, our observations) and occurs on several rust genera. ), clusters in that group, too. Moreover, in the infection experiments, we were not able to obtain Tuberculina infections of P. vincae from inocula other than T. sbrozzii. Consequently, T. sbrozzii, which was erected in 1899 for a Tuberculina specimen parasitizing Puccinia vincae (Cavara and Saccardo 1899), is presumably a monophyletic lineage, even though Helicobasidium purpureum appears then as paraphyletic in the molecular analyses. However, this might be due to lacking resolution of the DNA region.
Our results further suggest that lineages might have evolved that have lost the Helicobasidium-stage (Tuberculina maxima I, T. maxima II and T. sbrozzii). T. maxima II is common in Germany, but we were not able to detect any referring Helicobasidium specimen. The same is true for T. maxima I in North America. Both species parasitize rusts that are perennial, and both species are proven to be capable of overwintering as perennial mycelia with their rust fungal hosts in plant tissues and as spores (Wicker and Wells 1968, our observations). The capacity to overwinter might be due to the larger spores with thicker spore walls compared to Tuberculina persicina or T. sbrozzii. Thus, the soil-borne, perennial Helicobasidium-stage is not needed. In addition, Tuberculina sclerotia, the very structures that presumably mark the changeover from the Tuberculina- to the Helicobasidium-stage (Lutz et al 2004a), are unknown for T. maxima. The loss of the Tuberculina-stage involves a loss of sexual reproduction and consequently should result in a clonal population structure, which might be reflected by the uniformity of the ITS base sequences. Without exception the ITS sequences of T. maxima II specimens collected from northern Germany to southern Austria are identical, just as the T. maxima I sequences from North American specimens are. In that context, T. maxima I AY460135
[GenBank]
from Europe has to be assigned to a clone of itself. The sequences of the T. sbrozzii specimens collected in England, France, Germany, Italy and Madeira are identical too, it should be noted. In addition, their host rusts Puccinia cribrata and P. vincae are perennial (Gäumann 1959). T. sbrozzii possibly has evolved as clonal lineage accompanying P. vincae and closest relatives. The Tuberculina species that have lost the phytoparasitic Helicobasidium-stage still might be considered potential agents in biological rust control.
Our infection experiments finally reveal that not only Tuberculina conidia (cf. Barkai-Golan 1959, Vladimirskaya 1939, Wicker and Kimmey 1967) but also both Helicobasidium conidia formed in culture and basidiospores serve the same purpose: the infection of rust hosts. This might explain the observation of Ikeda et al (2003) that single basidiospore isolates of Helicobasidium mompa are not pathogenic with respect to plants; it also might explain the observation that, despite extensive research, no Helicobasidium infections of plants from inoculations with Helicobasidium basidiospores were reported.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Corresponding author. E-mail: matthias.lutz{at}uni-tuebingen.de
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