Evolution of trophic stages

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.

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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.



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.


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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.

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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


:Figs. neu kompr:18 Colacosome ontogeny2.png

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.


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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.


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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.


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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.

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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