Evolution of trophic stages

As heterotrophic organisms, fungi depend on organic nutrients, the substrate dependencies of their trophic stages is of utmost importance in their evolution. In this article, we can only focus on few selected examples to trace evolutionary trends. Animal associations are excluded. A simplified overview (Fig. 17) is used as a guideline for the following chapters.

Fig. 17. Evolution of Basidiomycota and distribution patterns of main trophic stages. Though the occurrence of principal nutritional dependencies in monophyletic groups of the Basidiomycota appears as randomly distributed, meaningful evolutionary trends can be detected. Mycoparasitism is widespread in Pucciniomycotina and dominant in the Tremellales, a basal taxon of the Agaricomycotina. The huge bulk of plant parasites belongs to the Pucciniomycotina and Ustilaginomycotina. However, important plant parasites occur scattered in diverse relationships of the Agaricomycotina. Animal associations are not included in this scheme. The phylogram is a compilation from data of various authors. Orig. F. Oberwinkler.

Evolutionary trends of Basidiomycota in trophic stages:

Mycoparasites > plant parasites > mycorrhizal associations

Plant parasites > saprobic stages

It can be deduced from Fig. 17 that mycoparasitism is a „fundamental initial motor in the basidiomycete evolution“ (Weiß et al. 2004a). Parasites of plants are most frequent in the Pucciniomycotina and Ustilaginomycotina. Parasites on woody plants are scattered in the Agaricomycotina. The most effective mycorrhizal radiation obviously occurred in the Sebacinales (Weiß et al. 2004b). Predominantly ectomycorrhizal partners constitute the Cantharellales, Gomphales, Hysterangiales, Thelephorales, Russulales, Boletales, and Agaricales. Dacrymycetales, Auriculariales and most of the Phallales are saprobic. Widely distributed are saprobic Basidiomycota also in the Hymenochaetales, Polyporales, Russulales, Atheliales, Boletales, and Agaricales.

Mycoparasitism

The highest diversity of mycoparasitic types is known from the Pucciniomycotina, comprising the three major basidiomycetous interfungal cellular interactions (Bauer 2004), colacosomes, nanometer-fusion, and Micrometer-fusion interaction. The nanometer-fusion type is also characterized by tremelloid haustoria. Only in the Tuberculina mycoparasites the Micrometer-fusion pores occur. In addition, penetration of host cells by cells of the parasite is found in few agaricoid species.

Fig. 18. Major types of cellular interactions in basidiomycetous mycoparasites. Colacosomes are exclusively known from members of the Pucciniomycotina. Cystobasidial and tremelloid haustoria are structurally very similar but occur in Pucciniomycotina and Agaricomycotina, respectively. The Tuberculina interaction with rust fungi is unique and only known from this genus. Cell penetration is known from the agaricoid mycoparasite Asterophora parasitica. The background of the figure illustrates the mycoparasitic interaction of a colacosome fungus with a Tulasnella host. TEM photos R. Bauer. Orig. F. Oberwinkler.

Evolutionary trends of basidiomycetous interfungal cellular interactions:

Origin unknown > colacosomes > loss of colacosomes

Origin unknown > nanometer-fusion interaction

Origin unknown > Micrometer-fusion interaction

Colacosome fungi

So far unknown subcellular bodies, responsible for mycoparasitic interaction, the colacosomes (Fig. 20), have been detected in Colacogloea peniophorae (Platygloea p., Oberwinkler et al. 1990a, Bauer & Oberwinkler 1991a), and at the same time in Cryptomycocolax abnormis (Fig. 19) with two different types (Oberwinkler & Bauer 1990). Colacosomes are exclusively known from Cryptomycocolacomycetes and Microbotryomycetes in the Pucciniomycotina. The phylogenetic distance between Cryptomycocolax and the colacosome fungi of the Microbotryomcetes, according to hypotheses based on molecular data, cannot be explained.

Fig. 19. Cryptomycocolax abnormis ecology and life cycle. a: Cirsium subcoriaceum. In old culms of this plant gelatinous pustles (b) were found on Mount Irazu, Costa Rica. c: Host-parasite-interaction through colacosomes; host hyphae without clamps, Cryptomycocolax hyphae with clamps. The host is forced to grow in the cells of the parasite. d: Basidial ontogeny: the primary phragmobasidium releases the upper cell, then the basal cell elongates and produces basidiospores apically. e: Simple septal pores associated with Woronin-like bodies. Orig. F. Oberwinkler and from Oberwinkler & Bauer (1990).

Evolutionary trends in colacosomes:

Original colacosome > two colacosome types > derived colacosome > loss of colacosome

Fig. 20. Left: Colacosomes in Cryptomycocolax abnormis (Oberwinkler & Bauer 1990). The host is an ascomycete that is forced to invaginate cells of the parasite. Right: Ontogeny of the derived colacosome type, deduced from Colacogloea peniophorae (Bauer & Oberwinkler 1991a). The scheme illustrates a series of developmental stages, beginning with an invagination of the plasmalemma of the parasite and ending with a fully developed colacosome. The chemical compounds involved in the penetration of the cell walls of the parasite and the host are unknown.

The colacosome with a central core surrounded by a membrane that finally fuses with the host plasmalemma, thus providing direct contact of host and parasite cytoplasm, was considered the ancestral one of the two types found in Cryptomycocolax abnormis (Oberwinkler & Bauer 1990). Derived colacosomes lack the pore, thus having lost the cytoplasmic fusion. They are the only ones occurring in the other colacosome fungi.

A second genus in the Cryptomycocolacomycetes, Colacosiphon, has been introduced by Kirschner et al. (2001). Structures that show colacosomes, but not recognized as such, were already reported by Kreger-van Rij & Veenhuis (1971) from Sporidiobolus. Also Atractocolax (Kirschner et al. 1999), Leucosporidium, Mastigobasidium, Rhodosporidium (Sampaio et al. 2003) are colacosome fungi.

Fig. 21. Basidio- and conidiocarps of Heterogastridium pycnidioideum. Left: anamorph stage, Hyalopycnis blepharistoma, in lateral view. Drawing: longitudinal section showing conidial stages. Right: mature basidium with tetraradiate basidiospores. Orig. F. Oberwinkler and from Oberwinkler et al.(1990b).

The anamorphic Hyalopycnis blepharistoma (Fig. 21) could be identified as a basidiomycete by Bandoni & Oberwinkler (1981), confirmed as such when the basidial stage, Heterogastridium pycnidioideum, was found (Oberwinkler et al. 1990b), and recognized as a mycoparasite when colacosomes were detected (Bauer 2004).

Based on molecular phylogenetic hypotheses, Heterogastridiales and Leucosporidiales cluster with the plant parasitic Microbotryales, the false smuts. In the latter no mycoparasites are known.

Tremelloid haustoria

Short hyphal branches, subtended by a clamp, basally swollen and apically tapering into a narrow filaments that can protrude hyphal walls and interact with the host cytoplasm through nanometer-pores are representative for Tremella species (Fig. 22). Tremelloid haustoria are frequent in Tremellomycetes (Figs. 23, 24), and they are typical also for several mycoparasites in the Pucciniomycota, e. g. species of the genera Classicula of the Classiculales (Bauer et al. 2003), Cystobasidium (Sampaio & Oberwinkler 2011) and Occultifur (Oberwinkler 1990) of the Cystobasidiales, Spiculogloea (Langer & Oberwinkler 1998) of the Spiculogloeales, or Zygogloea (Bauer 2004).

The convergent evolution of the tremelloid haustorium in Pucciniomycotina and the Tremellomycetes of the Agaricomycotina cannot be explained.

Fig. 22. Ontogeny of Tremella. The dimorphic and bitrophic life cycle of tremelloid fungi is compiled in this scheme. Basidiospores germinate by budding, by producing secondary spores or occasionally by hyphae. The yeast phase is saprobic. Conjugation of compatible yeast cells is initiated by tremerogens, followed by hyphal growth. Tremelloid haustoria develop early in ontogeny, sometimes already in the yeast stage. Mycoparasitic interactions occur when adequate hosts are available. Hyphal septa are characterized by tremelloid dolipores with specific tubular parenthesome cisternae. Asexual propagation with conidia occurs before or during basidiospore development. Most tremelloid species have gelatinous hyphal systems and basidiocarps. Modified from Oberwinkler (2009).

Evolutionary trends in tremelloid haustoria:

A common origin for nanometer-fusion mycoparasites of the Pucciniomycotina and the Tremellomycetes or a convergent evolution has been discussed by Bauer (2004). There is no possibility, so far, to understand evolutionary trends in tremelloid mycoparasites.

Fig. 23. Morphology and mycoparasitism of Tremella encephala on Sterum sanguinolentum. The parasite forces the host to grow hypertrophically. Host hyphae broad and without clamps, Tremella hyphae narrow and with clamps, haustorial attachments marked with arrow-heads. The gall-like to cerebriform growth is the result of a hyphal mixture of both fungi. The gelatinous Tremella hymenium is on the periphery of the galls. Orig. F. Oberwinkler.

Fig. 24. Life cycle and mycoparasitism of Christiansenia pallida on Phanerochaete cremea. Monokaryotic basidiospores bud and produce yeast colonies. Compatible yeast cells conjugate and grow with dikaryotic hyphae that produce tremelloid haustoria. Dikaryotic conidia predominantly develop in the parasitic stage, continue to grow with dikaryotic hyphae or dedikaryotize and then begin to bud. Basidia are suburniform and often more than four-spored. Strongly modified from Oberwinkler et al. (1984).

Some additional mycoparasitic interaction types

The micrometer-fusion type

Lutz et al. (2004a,b) were able to experimentally prove that Tuberculina, mycoparasitic on rust fungi, is a developmental stage of the plant parasite Helicobasidium. Micromorphological and molecular data indicate that the Helicobasidiales are closely related with the Pucciniales. Unique micrometer-fusion channels between host and parasite cells potentially allow the transfer of cell organelles (Bauer & al. 2004). Infection experiments revealed a high diversity in host specifity (Lutz et al. 2004c), probably indicating coevolutionary processes.

Intracellular haustoria with nanometer-fusion

Based on unique micromorphological characters, the mycoparasitic Platygloea sebacea has been transferred in an own genus, Naohidea (Oberwinkler 1990). Bauer (2004) found intracellular haustoria with nanometer-fusion pores, typical for tremelloid haustoria. Evolutionary trends are not recognizable in the Naohidea mycoparasitism.

Intracellular haustoria with unknown interaction

The agaricoid Asterophora species grow on Lactarius and Russula hosts, often in old and decaying basidiocarps. Therefore, they are mostly considered as being saprotrophic. However, already in young developmental stages, inter- and intracellular hyphae of the mycoparasite are present in host cells. Specific haustorial structures are absent. The ultrastructure of interactive structures has not been studied.

Up to 15 species are known in the mycoparasitic genus Squamanita (Matheny & Griffith 2010) of the Cystodermateae in the Agaricales. The authors found that S. paradoxa is a specific mycoparasite of Cystoderma amianthinum. Squamanita odorata is known as a parasite of Hebeloma mesophaeum (Mondiet et al 2007), and S. umbonata occurs on Inocybe oblectabilis (Vizzini & Girlanda 1997). Matheny & Griffith (2010) conclude that up to five species of Squamanita may parasitize closely related species, given that the molecularly based phylogenetic hypothesis is correct. In mycoparasitic Squamanita species no data are available concerning the cellular interactions of parasite and host.

The few mycoparasites known in the Boletales will be briefly mentioned later when mycorrhizae and their swiches to other nutrional modes are discussed.

Evolutionary trends in parasitic Agaricales:

Origin polyphyletic > hostrange restricted to mushrooms > hostrange restricted either to Agaricales or Russulaceae

Fig. 25. Morphology and mycoparasitism of Asterophora parasitica on Russula nigricans. a young basidiocarp. b early developmental stages of lamellae. c mature basidiocarp. d colony of basidiocarps in different developmental stages, growing on the lamellae of the host. e hymenium and subhymium with chlamydospores. f and g hyphae of the parasite in the host. Orig. F. Oberwinkler.

Plant parasites

Plants are the key players in fungal evolutionary processes. Interactions between plants and fungi are manifold, but terminologically reduced to few categories, like symbiosis, mutualism, parasitism, saprophytism, or endophytism. More specific categories were chosen for this overview (Fig. 17). In all three subdivisions of Basidiomycota, plant parasites are widely distributed and ecologically of particular importance. Pucciniales, Microbotryomycetes, Ustilaginomycotina, Polyporales, Hymenochaetales and Russulales constitute the dominant plant parasites in the Basidiomycota.

Pucciniales (Uredinales), rust fungi

The most important fungal plant parasites are the rust fungi. They have a worldwide distribution and occur on ferns and seed plants with approximately 8000 species. Their whole life cycle depends on parasitic interactions and many species have obligatory host alternations.

The origin of the Pucciniales is unknown, their evolutionary trends in life cycles and host dependencies are partly well explored and experimentally proven. Molecularly based phylogenetic hypotheses can be tested for their reliability concerning coevolutionary processes in rust fungi and their host plants.

The so-called „typical rust fungus life cycle“ is the one of Puccinia graminis, the black stem rust of grasses (Fig. 26). Because there are many other rust fungi with equivalent ontogenies, it makes sense to briefly explain this life story. There are five very important strategies involved: (1) all developmental stages are parasitic ones, (2) the haplophase depends on another host than the dikaryophase, (3) the aeciospores initiate the host alternation, (4) the urediniospores spread out the pathogen on the host for the dikaryophase, (5) the sequence of spore generations is fixed, irrespective of losses of them.

Fig. 26. The typical life cycle of rust fungi, as in Puccinia graminis. Basidiospores (IV) infect the specific host for the haplophase. Monokaryotic pycniospores (0) develop and can fertilize aeciospore intitial stages on the same host. This process results in dikaryotic aeciospores (I). Aeciospores are no more able to infect the host on which they were produced. In contrast, they have to be distributed randomly for finally reaching their specific second host. On that one, vegetative propagules, the urediniospores (II) are developed in quantities for the purpose of effective distributing the dikaryophase. Finally, the teliospores (III) develop on the same host. They are probasidia, i.e. karyogamy occurs in their cells. Teliospores germinate to produce meiosporangia and basidiospores that terminate the ontogenetic cycle. Orig. F. Oberwinkler.

Evolutionary trends in rust fungal host dependencies:

Primary autoecious (hypothetical) > heteroecious > autoecious

Host alternations > only one host

The following discussion refers basically to Pucciniales distributed in the northern hemisphere. Data were mostly extracted from Gäumann (1959), Poelt & Zwetko (1997), and Zwetko & Blanz (2004) over a long time, and condensed to schemes for teaching purposes.

Primary autoecious rust fungi are not known but they must have existed because heteroecism requires simpler ancestors. In a molecular phylogenetic hypothesis of Aime (2006) the anamorphic rust fungus Caeoma torreyae is in a basal position, followed by a clade containing Mikronegeria alba, Blastospora smilacis, Hemileia vastatrix, and Maravalia cryptostegiae. – It was convincing to assume that the rust lineage begins with fern rusts, however, they have host alternations restricted to Abies species in the haplophase. A cladistic approach to the question „do primitive hosts harbor primitive parasites?“ (Hart 1988) excluded fern rusts from basal phylogenetic positions. The first molecularly based phylogenetic studies of rust fungi comprising fern rusts (Sjamsuridzal et al. 1999, Maier et al. 2003) confirmed the cladistic findings.

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Fig. 27. Host dependencies and life cycles of rust fungi, Pucciniales. Primary autoecious rust fungi are not known. Conifers are most important hosts for haplophases of rust with alternations to ferns and angiosperms, harboring the dikaryophases. Secondary autoecious rusts evolved in many convergent lineages from orginally heteroecious ones. Strongly modified after Oberwinkler (2009). – The life cycle variations are shown in the diagram to the right and will be explained below as evolutionary trends. 0 – Pycniospores, I – Aeciospores, II – Urediniospores, III – Teliospores, IV – Basidiospores. Autoecious life cylce 0-IV: yellow – green, heteroecious life cycle 0-IV: green. White boxes without numbers: spore generation lacking.

Evolutionary trends in life cycles:

Autoecious (hypothetical) > heteroecious > autoecious

Eu-type 0, I, II, III, IV: heteroecious > autoecious

Aecididal repetition 0, I, I, I, II, III, IV: heteroecious > autoecious

Opsis-type 0, I, III, IV: heteroecious > autoecious

Brachy-type 0, II, III, IV: autoecious

Mikro-type (0), III, IV: autoecious

Endo-type (0), I, IV: autoecious

Only few examples are given for the different life cycles:

• Eu-type, heteroecious: Puccinia graminis, Cronartium ribicola and many others.

• Eu-type, autoecious: Phragmidium spp.

• Aecidial repetition, autoecious: Phragmidium mucronatum

• Opsis-type, heteroecious: Gymnosporangium spp.

• Opsis-type, autoecious: Uromyces primulae-integrifoliae

• Brachy-type, autoecious: Frommea obtusa, Kuehneola uredinis, Trachyspora intrusa

• Micro-type, autoecious: Puccinia aegopodii, P. malvacearum

• Endo-type, autoecious: Endocronartium spp., Endophyllum spp.

Tranzschel’s rule describes a reductive coevolutionary trend: micro-type rusts live on aecial hosts of their closely related heteroecious eu-type species. The following examples can document this evolutionary process.

• Chrysomyxa rhododendri heteroecious: 0, I on Picea, II, III on Rhododendron

• Chrysomyxa abietis microcyclic: III on Picea

• Tranzschelia pruni-spinosae heteroecious: 0, I on Anemone, II, III on Prunus

• Tranzschelia fusca microcyclic: III on Anemone

• Uromyces rumicis heteroecious: 0, I on Ficaria, II, III on Rumex

• Uromyces ficariae microcyclic: III on Ficaria

• Puccinia coronata heteroecious: 0, I on Poaceae, II, III on Rhamnus

• Puccinia mesnieriana microcyclic: III on Rhamnus

The genus Melampsora can serve as a model taxon for documenting major evolutionary and coevolutionary trends in the Pucciniales (Fig. 28). Primary hosts for the haplophase are species of the conifer genera Abies, Larix, Pinus, and Tsuga in the Pinaceae. The original heteroecious Melampsora species were heteroecious with the dikarophase on species of Populus and Salix of the Salicaceae. Species were then evolved with host alternations to various other Angiosperms, using these as hosts for their haplophase. Finally, heteroecism broke down, and autoecious species evolved with effective radiation on closely related hosts, e.g. Euphorbia. Remarkable is that the transition from heteroecism to autoecism also occurred on the primary hosts for the haplophase, as documented by Melampsora farlowii on Tsuga canadensis and T. caroliniana in eastern North America (Hepting & Toole 1939). In phylogenetic hypotheses based on molecular data (Maier et al. 2003, Pei et al. 2005, Aime 2006), Melampsora is confirmed as a monophylum.

Fig. 28. Evolutionary steps in life cycles and host dependencies of Melampsora species. Evolutionary trends in this model genus of rust fungi are: primary heteroecious > secondary heteroecious > autoecious. The loss of a host alternation can also happen on Tsuga, the primary haplophase host. Illustrations from Fischer 1902, Hunter 1936, Mayor 1920, Sappin-Trouffy 1896. Orig. F. Oberwinkler.

A second example of rust fungi with host alternations from conifers to angiosperms is illustrated in Fig. 29 for the Mikronegeriaceae and Pucciniastraceae. – Two Mikronegeria species, M. fagi and M. alba, with their dikaryophase on Nothofagus are known from southern South America (Butin 1969, Peterson & Oehrens 1978). The haplophase of M. fagi grows on Araucaria araucana, the one of M. alba on Austrocedrus chilensis. Crane & Peterson (2007) were able to experimentally prove the host alternation of a third species in New Zealand, M. fuchsiae, growing on Phyllocladus spp. in the haplophase and Fuchsia excorticata, F. perscandes and the introduced F. magellanica in the dikaryophase. – Melampsoridium rusts are restricted in the haplophase to Larix hosts and grow in the dikaryophase on species of the Betulaceae. – Abies species harbor the haplophases of Pucciniastrum and Melampsorella rusts. Caryophyllaceae serve as the exclusive hosts for the Melampsorella dikaryophase, while Pucciniastrum species occur in their dikaryophase on host species of the Onagraceae, Rosaceae, Hydrangeaceae, and Malvaceae (Sterculiaceae and Tiliaceae), and autoecious species live on Orchidaceae. In his Pucciniastrum monograph, Naohide Hiratsuka (1927) characterized the genus by „Uredolager von einer halbkugeligen oder kegelförmigen Pseudoperidie umschlossen, die sich mit einem scheitelständigen Porus öffnet.“ Teliospores are thin-walled and grouped in subepidermal layers, this in contrast to Thecaphora species with intracellular telia. Aecia of Thecaphora species are grouped, covering the inner surface of cone scales of Picea species.

Fig. 29. Rust fungi of the Mikronegeriaceae and Pucciniastraceae with haplophases on conifers and host alternations with various Dicotyledons. The three Mikronegeria rust fungi are restricted to southern South America and New Zealand, Pucciniastraceae are distributed in the Northern Hemisphere within the distribution range of Abies, Larix, Picea and Tsuga species. Illustrations from Fischer 1902, Hunter 1936, Pady 1933, Sappin-Trouffy 1896, and Oberwinkler.

The origin and the driving forces for the evolution of host alternations in rust fungi are unknown. Because of this unique life strategy, it seems convincing to predict one common ancestor for the Pucciniales. Their main evolutionary radiation, both as heteroecious and autoecious parasites was closely connected with the evolution of their hosts, the seed plants. A rich diversivication took place on coniferous hosts (Figs. 28, 29, 30). Few additional examples will be briefly mentioned (Fig. 31).

Cronartium is characterized by long columns of teliospores. The haplophase only occurs on Pinus species. Most of the hosts for the dikaryophase belong to the Lamianae of the Asteridae, predominantly species of genera in the Apocynaceae, Gentianaceae and Orobanchaceae, but also in Fagaceae, Balsaminaceae, Paeoniaceae and Grossulariaceae. Cronartium ribicola is restricted to fife-needle pines, other species develop their haplophase on two-three-needle pines. A special reduction of the life cycle occurred in Endocronartium with heterocious species and an endo-type life cycle (Fig. 27).

The haplophase of Chrysomyxa species is restricted to Picea. Ericaceae, inclusive of the former Empetraceae and Pyrolaceae are the exclusive host groups for the dikaryophase. An autoecious species is Chrysomyxa abietis on Picea abies.

Basidia with mucous caps are replacing teliospores (III) in Coleosporium. Heteroecious species have a host alternation between Pinus species for the haplophase and mainly species of the Asteridae (Apocynaceae, Rubiaceae, Orobanchaceae, Lamiaceae, Campanulaceae, Asteraceae) and some Ranunculaceae. Coleosporium is also reported as autoecious from Orchidaceae.

Fig. 30. A hypothesis of rust fungal coradiation with plants in evolving vegetation types of the Northern Hemisphere. Yellow ellipses show the host groups for haplophases, red ellipses those for the hosts harboring the dikaryophase stages. (1) The origin of Pucciniales as autoecious and/or as heteroecious plant parasites is not known. The extant fern rusts are not the ancestors of rust fungi according to molecular phylogenetic hypotheses. (2) Heteroecious fern rusts live in coniferous climax vegetations because they depend on Abies species as exclusive hosts for their haplophases. The restriction of the haplophase to one genus of the conifers cannot be explained. Autoecious fern rusts are also known outside the geographical range of Abies, for example in the Southern Hemisphere. (3, 4) Gymnosporangium rusts are exceptional because of a unique host dependency with the dikaryophase on conifers, i.e. exclusively on Cupressaceae. All hosts for the haplophase are species of the Rosaceae-Maloideae, except very few members of the Hydrangeaceae including Philadelphaceae, Juglandaceae, and Myricaceae. No explanations can be given for the origin and the host selectivity of Gymnosporangium. Woodlands with Juniperus and species of the Maloideae are a prerequisite for Gymnosporangium development and coevolution. (5, 6) A high diversity of Puccinia and Uromyces evolved on Poaceae as hosts of the dikaryophase. Associated woody plants of the Berberidaceae, Rhamnaceae, and Caprifoliaceae are possibly primary hosts for the haplophase. (7) Many herbaceous species of the Dicotyledons, e.g. Ranunculaceae, Crassulaceae, Oxalidaceae, Boraginaceae, Apiaceae, Asteraceae, and of the Monocotyledons served as hosts for the haplophases. (8) Numerous secondary autoecious species resulted in close coevolutionary processes, e.g. Uromyces on Fabaceae. (9) The origin of heteroecious rusts with their dikaryophases on Cyperaceae, mainly on Carex, is not known. Their hosts for the haplophases are richly diversivied on Asteraceae, but occur also on Orobanchaceae, Primulaceae, Urticaceae, Celastraceae (Parnassia), Onagraceae, and Grossulariaceae. Microcyclic derivatives evolved frequently in the Asteraceae. The Puccinia-Uromyces relationship coevolved with grasslands and vegetations dominated by herbaceous plants. – The red arrows point to the positions of two economically important rust species, the black or stem rust of grasses, including cereals, Puccinia graminis, and the pear rust, Gymnosporangium sabinae. Orig. F. Oberwinkler.

The first representative phylogenetic hypothesis of the Pucciniales, based on molecular data (Maier et al. 2003), documented the common origin of Puccinia, Uromyces, Endophyllum and Cumminsiella, and the monophyly of the autoecious rusts on Rosaceae Phragmidium, Kuehneola, Triphragmium and Trachyspora. Also each of the genera Chrysomyxa, Coleosporium, Cronartium, Gymnosporangium, Melampsora, Phragmidium and Tranzschelia, as well as the Pucciniastreae sensu Dietel, are monophyletic.

Fig. 31. Simplified phylogeny of selected genera of the Pucciniales and few related parasitic fungi of the Pucciniomycetes, based on morphological and life cycle characters. In species of the Pucciniomycetes hyphae have no clamps, septal pores are often associated with microbodies and intermeiotic SPB duplication occurs typically in metaphase (Bauer et al. 2006). Essential assumptions are primarily autoecious and subsequent heteroecious ancestors for the Pucciniales. Teliospores are thin-walled and hyaline in basal rust fungi and thick-walled and pigmented in derived ones. Melampsora is characterized by aecial caeomata and uredinial capitate paraphyses. Pucciniastrum has uredinial peridia with ostiolar cells. Uredinopsis, Cronartium, Chrysomyxa, and Coleosporium share the common feature of velopedunculate haustoria (Berndt 1996, Berndt & Oberwinkler 1997). Carotinoids are common in rust fungi, however, they are lacking in the fern rust Uredinopsis. An aecial peridermium is a synapomorphy for Cronartium, Chrysomyxa, and Coleosporium species. Urediniospores can be considered secondary aeciospores in Chrysomyxa and Coleosporium. Coleosporium basidia have mucous terminal parts and they replace teliospores (III) what has been interpreted as internal germination. Puccinia and Gymnosporangium share two-celled teliospores while Phragmidium has pluricellular ones. – Further mutualists within the Pucciniomycetes comprise the plant parasitic Platygloeales with Eocronartium in the diagram, and parasites of scale insects, the Septobasidiales. Orig. F. Oberwinkler.

Plant parasites related to rust fungi

Besides rust fungi, Pucciniomycotina comprise additional plant parasites with particular importance for the understanding of evolutionary trends. This may be the case for the Herpobasidium relationship (Fig. 32), now named Platygloeales. All species in this group share unclamped hyphae, simple septal pores, and auricularioid basidia with an active spore release. Considering host dependencies, the sequence of major steps was from mosses to ferns and seed plants. Oberwinkler & Bandoni (1984) revised the fern parasitic species of Herpobasidium and Platycarpa, introduced Ptechetelium cyatheae, also on ferns, and Insolibasidium deformans growing on species of Caprifoliaceae. In a phylogenetic hypothesis, based on molecular data (Aime et al. 2007), the Platygloeales contain Platygloea, Insolibasidium, Eocronartium, and Jola. Herpobasidium, Platycarpa, Ptechetelium and Paraphelaria were not included in this study.

Fig. 32. Representatives of the Platygloeales arranged according to the phylogeny of their host plants. The tropic and subtropical Jola species produce gelatinous pustules around spore capsules of mosses (Bryopsida). Eocronartium is clavarioid and arises from the gametophyte or sporophyte initials of mosses. The ramarioid Paraphelaria amboinensis grows on roots of bamboos in Southeast Asia. The parasites on ferns, Herpobasidium, Platycarpa, and Ptechetelium, as Insolibasidium on Caprifoliaceae, have resupinate fructifications. Orig. F. Oberwinkler.

Possible evolutionary trends in plant parasites related to rust fungi:

Coevolution with the hosts: on mosses > ferns > seed plants

Basidiocarps inconspicuous resupinate > clavarioid > ramarioid

Because of insuffient sampling, molecular phylogenetic hypotheses are fragmentary and cannot yet be used for testing the above mentioned evolutionary trends.

Microbotryomycetes, false smuts and related fungi

Basidiomycetous fungi with basically different trophic requirements are included in Microbotryomycetes. Heterogastridiales contain mycoparasites with colacosomes (see colacosome fungi), the teleosporic Leucosporidiales and Sporidiobolales also have colacosomes, but are not considered to be mycoparasitic. The plant parasitic false smuts, Microbotryales have smut spores but no colacosomes.

The ontogeny, including trophic stages, of Microbotryum (Fig. 33) is for the most part a duplication of the Ustilago life cycle. Such comprehensive convergency is rare and may be compared in basidiomycetous fungi only with the multiple and independent evolution of agaricoid basidiomata.

When studying anther smuts of the Caryophyllaceae, Deml & Oberwinkler (1982), became aware of the heterogeneity of so-called Ustilago species. To accomodate Ustilago violacea, they reintroduced Microbotryum, a genus erected by Léveillé already in 1847. Since then Microbotryum violaceum has become a model organism for studies in coevolution of plant pathogens and their hosts as well as in population genetics.

The following discussion refers on coevolutionary aspects of Microbotryum s.l. and the host plants.

Fig. 33. Life cycle of Microbotryum violaceum. In most Microbotryum species, smut spores (teliospores, probasidia) are developed in the anthers of their hosts. They germinate with basidia and bud off basidiospores, also called sporidia (left). Budding continues and yeast colonies develop, representing the saprobic stage (right). After conjugation of compatible yeasts, hyphae develop and infect suitable hosts. Smut spores originate inside hyphae in specific organs of the host. Orig. F. Oberwinkler.

Fig. 34. Specific host dependencies in Microbotryum s.l. on members of the Asteridae. Both, hosts and parasites are monophyletic. However, Microbotryum onopordi is not congruent with the Asteraceae clade. The tree is part of a strict consensus of 1780 most parsimonious trees inferred from the dataset consisting of three concatenated, complete ITS alignments. Symbols on branches indicate the magnitude of parsimony bootstrap values from analyses of the dataset after exclusion of alignment-ambiguous sites (upper left) and of the three different, complete alignments made with MAFFT (upper right), PCMA (lower left), and POA (lower right), from Kemler et al. (2006). – Microbotryum pinguiculae sporulates in the anthers of Pinguicula alpina, M. salviae (betonicae) in the anthers of Salvia pratensis, and M. tragopogonis-pratensis in the flower head of Tragopogon pratensis. Photos orig. F. Oberwinkler.

Evolutionary trends in Microbotryum:

The following remarks refer to the studies of Kemler et al. (2006, 2009).

Hosts Polygonaceae > Caryophyllaceae > Asteridae

Sporulation on leaves > flowers > in anthers > in inflorescences

Host specificity broad? > narrow (specific) > one host with several parasites

Molecular hypotheses are in favor for an origin of Microbotryaceae on Polygonaceae. Overlapping host ranges were found in Fallopia. In the Caryophyllaceae, Microbotryum appears monophyletic, with a strong tendency for species specificity, and sporulation in the anthers. This is also the case in members of the Portulacaceae, Lamiaceae, Lentibulariaceae, and Dipsacaceae. Kemler et al. (2006) assume that there may be two independent lineages of anther smuts. Cryptic species, undetectable with morphological studies remain to be discovered with molecular methods.

The term host specificity is not fully adequate to evolutionary specialization concerning host dependencies. The anther-smuts are an excellent example for organ specificity of the sporulation place including functional aspects of dispersal efficiency. In the case of Ustilentyloma fluitans, (Fig. 35 a), growing in Glyceria fluitans, and Kriegeria eriophori in Scirpus sylvaticus (Fig. 35 b), leaf aerenchyma of the hosts serve as ecological niches for the development of the parasites.

Fig. 35 a. Kriegeria eriophori in Scirpus sylvaticus. The parasite grows in host leaf aerenchyma. Probasidia develop inside and basidia outside of the leaf. Basidia are deciduous and can float away in the water surrounding the host plant. b. Ustilentyloma fluitans in Glyceria fluitans. Full development of smut spores and basidia takes place in the aerenchyma chambers. Orig. F. Oberwinkler

Ustilaginomycotina, true smuts and related fungi

A highly diverse grouping of basidiomycetous fungi constitutes the Ustilaginomycotina as one of the three subdivisions in the Basidiomycota, commonly accepted at present. To verify this assemblage as a monophylum is challenging. Prillinger et al. (1990, 1993) found that the carbohydrates of these fungi are rich in glucose but lack xylose, thus distinguishing them from Pucciniomycotina and Agaricomycotina. A representative survey of septal pore types (Bauer et al. 1997, 2006) recognized membranous pore caps, and vesicle derived host-parasite interactions (Bauer et al. 1997), both most likely synapomorphies (Fig. 36). Finally, phylogenetic hypotheses, based on sequence data were taken as conclusive results. The first ones were especially remarkable because they distinguished between secondary structures of the 5S rRNA (Gottschalk & Blanz 1985). They found that the true smuts share the type B of the 5S rRNA with the Agaricomycotina. The monophyly of the Ustilaginomycotina was confirmed in later studies, but depending on sampling and sequences used, the support values varied considerably. Actually, the Ustilaginomycotina are treated without Entorrhiza by phylogenists, using molecular data, (e.g. Hibbett et al 2007).

Only some evolutionary trends of true smuts and related ​​ fungi will be discussed here, following the arrangement of orders as in Fig. 36.

Fig. 36. Phylogenetic hypothesis for the Ustilaginomycotina, strongly modified after Bauer et al. (1997). Because nearly all smut fungi parasitize on angiosperms, a geological time table is added for the period in which the host plants evolved. Based on ultrastructural and molecular data, partly also on basidial morphology, the Ustilaginomycotina are divided in two classes, the Ustilaginomycetes and the Exobasidiomycetes. Representative septal pore types and basidia are illustrated, as well as few host-parasite interphases. In addition, the occurrence of teliospores is marked by red-yellow circles. Included are also the anamorphic Malasseziales. TEM pictures orig. R. Bauer, drawings orig. F. Oberwinkler