Phylogeny of Fungi
Introduction
Precise phylogenetic history of the fungi can be open to various interpretations and has been an inexact science at best. This is mostly due to their poor fossil records. Unlike many other organisms, fungal structures do not fossilize well and we have little data on which to base theories of phylogeny. Thus, when mycologists began theorizing about the phylogeny of fungi, it was based only on the morphological features of extant fungi. As you might expect, this led to a number of subjective ideas in the phylogeny of fungi, many of, which are no longer, followed. In discussing this subject, it is probably best to approach it from a historical perspective so that you can see how mycologists have changed their ideas as new information was gathered from new tools that have been developed over the last forty years.
The Monophyletic Origin of Fungi
The monophyletic origin of "fungi" is the dogma that most mycologists followed since the beginning of the 20th. Century (Atkinson, 1915; Gäuman and Dodge, 1928; Luttrell, 1955; Savile, 1968) and earlier. In this theory, it is assumed that all the fungi were derived from an algal ancestor that lost its ability to photosynthesize. This gave rise to the flagellate fungi. A fungal ancestor then gave rise to the rest of the fungi, and usually this ancestor was assumed to be a member of the Chytridiomycota, which was morphologically similar to their modern counterparts and produced posteriorly, uniflagellated zoospores. Like many of its modern counterpart, this ancestral chytrid was aquatic, but over time, became more adapted to the terrestrial environment.
The loss of flagella and the evolution of the zygospore gave rise to the Zygomycota. How this was to have occurred is never addressed and there has never been a hypothetical, intermediate ancestor proposed. Recall that this phylum has nonmotile, asexual sporangiospores (asexual spores borne in a sporangium), and in one line multinucleate zygospores, which are sexual spores that arise through fusion of gametangia,e.g. Rhizopus stolonifer. The most primitive member of this line of Zygomycota was believed to be morphologically similar to Mucor or Rhizopus, which produce large, single, multispored, columellate sporangia. As this group evolved, the number of sporangiospores in a sporangium became reduced and the columella was lost, thereby the sporangiole was evolved, with the most advance members producing single-spored sporangioles, e.g. Cunninghamella. This led to the evolution of the conidium, an asexual spore typically produced by the Ascomycota and Basidiomycota where an anamorph stage is produced. Another line that arose within the Zygomycota was that which included the Endogonales. The zygospores produced in this line were uninucleate. This line was believed to have given rise to the Ascomycota.
The link between the Zygomycota and Ascomycota was made between a fungus that resembled Dipodascopsis (Ascomycota). Morphologically, its gametangia are similar to those in Endogone and each produces a uninucleate zygote, within a saclike structure. The germ sporangium and ascus in these species are thought to be homologous. However, free cell formation occurs in Dipodascopsis and is absent in Endogone. The Dipodascopsis-like ancestor was thought to be a pivotal organism, which through reduction gave rise to the unicellular yeasts and to a more complex filamentous Ascomycota. The latter gave rise to an extended dikaryotic stage, which is believed to be similar to the modern day Taphrina. The Taphrina-like ancestor gave rise to the remaining members of the Ascomycota, which produce ascocarps, in two divergent lines; one producing the unitunicate ascus and the other the bitunicate ascus.
The Taphrina-like ancestor was also believed to have given rise to the ancestral Basidiomycota, which diverged into two lines. One line produced a microcyclic rust, which produced only teliospores and basidiospores and led to the present-day rusts. The other line produced the ancestor of the present day Auriculariales, which had a poorly differentiated basidiocarp and transversely septate mycelium. This line gave rise to the remaining basidial and basidiocarp types in the Basidiomycota.
There were, as you may expect, variations to the above phylogeny and inclusion of other groups that were excluded. Some variations regarding specific taxa will be discussed.
Some Variations to the Monophyletic Origin of the Fungi
George W. Martin (1932; 1960) put forth some convincing argument as to the fungal nature of the Myxomycetes. He and Macbride (1899) were two of the few modern mycologists to believe in the relationship of this group to fungi. Link (1833) was the first mycologists to classify this group with the fungi. It was he that coined the term Myxomycetes (literally slime fungus). However, as early as 1887, de Bary had already considered them animals and had classified them as such by calling them Mycetozoans (literally, fungus animal) and his classification was followed by Bessey (1950) and Kudo (1954). That they continued to be associated with the fungi can be credited to MacBride and Martin who had made significant contributions to the study of Myxomycetes. Olive (1970; 1974) believed that the other slime molds, the Acrasiomycota and Dictyosteliomycota were also related to the Myxomycota and that they formed a monophyletic group.
Bessey (1950) believed that the Zygomycota were derived from the Oomycota rather than Chytridiomycota, based on similarities in morphology of their sporangia and that both phyla produced coenocytic mycelium.
Sachs (1874), Bessey (1950) and Denison and Carrol (1966) believed that the Ascomycota were derived from the Floridean Red Algae (Rhodophyta). Although Kohlmeyer (1973) did not advocate the direct derivation of the Ascomycota from the Rhodophyta, he postulated a hypothetical, common ancestor that gave rise to both phyla. Demoulin (1974) had a similar hypothesis, but believed that both the Ascomycota and Basdiomycota were derived from a red algal ancestor. In all of the above theories, there was a great deal of emphasis placed on what were thought to be homologous structures in the life cycles of the Rhodophyta and filamentous Ascomycota that produce ascocarp, and in the case of Demoulin, a comparison between the structures in the rust life cycle and the Rhodophyta, as well.Bessey (1950) further postulated an interesting phylogeny within the Ascomycota. He believed the most primitive members were those that produced the ascocarps and the most advanced members were the ascosporogenous yeasts, e.g. Saccharomycetales. Thus, he thought the most primitive members produced apothecia and that perithecia and cleistothecia arose later, and as the Ascomycota continued to evolve, the ascocarp was eventually lost from the life cycle. Bessey's reasoning was that since the Ascomycota members that produce ascocarps had structures that were homologous to the Rhodophyta, they must be the primitive members. There were not a lot of mycologists that followed this theory, but some of these were very vocal where this theory was concerned, which probably led to the persistence of this theory.
Changes in Ideas in Theories of Phylogeny in the Fungi
Until the 1960's, the monophyletic origin of the fungi was followed by most mycologists, with a small handful advocating a polyphyletic origin, with the red algal origin of the Ascomycota. During this decade, characteristics not previously incorporated into determining fungal phylogeny and new tools that became available brought forth new theories on the interrelationship of the different fungal taxa. Some new criteria that were considered in fungal phylogeny included:
The removal of the Oomycota from the fungi was not a new idea, but it was not until Whittaker (1969) that this group of fungi was formally separted from the fungi. By this time there was already a large body of evidence that warranted reclassification of this phylum; the Oomycota have cell walls composed primarily of cellulose, mitochondria with tubular cristae and lysine is synthesized by way of the a aminoadipic acid (AAA) pathway. In the fungi, cell walls are primarily chitin, their mitochondria have plate-like cristae and lysine is synthesized via the diaminopimelic acid (DAP) pathway. In addition, there are a number of morphological features that differ from other fungi. Pringsheim (1858) and Kriesel (1969) went so far as to classify this group with the Chrysophyta ( the yellow brown algae). However, most other mycologists were still uncertain at that time as to their relationship to. Other flagellates, i.e. Hyphochytriomycota, Chytridiomycota, Plasmodiophoromycota (a group we didn't cover), at this time were now also believed to be of independent origin, based on some of the above features.
Whittaker's five kingdom system, which was adopted by most researchers, also reclassified the slime molds into a different kingdom as well. This officially separated the fungi into two kingdoms: All the flagellate fungi, including the Chytridiomycota, and slime molds were placed in the Kingdom Protista and the remainder in the Kingdom Myceteae.
The placement of the Trichomycetes, in the Zygomycota, has never been a good fit. Many of its members are not known to produce zygospores and were placed there based on their habitat rather than morphology. They were assumed to be polyphyletic in origin by this time. The cell wall composition in Amoebium, for example was different from that of any of the types of cell walls identified for other taxa of fungi.
The "slime molds" at this time were thought to be a monophyletic group, based on the amoeba stage that germinated from spore and consumed nourishment via phagocytosis. However, that these organisms were related to the fungi was finally laid to rest. Most mycologists had not recognized slime molds as being related to fungi for quite some time.
Modern Hypotheses on the Phylogeny of Fungi (According to Mims and Blackwell)
With the advent of molecular techniques, hypotheses of phylogeny among the various groups of fungi changed radically. We have covered many of these changes. Lets review the different fungal groups that we have covered this semester.
The "slime molds", Acrasiomycota, Dictyosteliomycota and Myxomycota are currently thought to be unrelated groups despite the fact that all three phyla produce amoebae from spores that feed via phagocytosis. However, this conclusion was not based on moleculear evidence. Because the amoebae feed on bacterial cells, their DNA persist throughout the life cycle of the slime molds, making it impossible to obtain pure genomic samples of slime molds. As already mentioned above, with the exception of Martin and MacBride, most mycologists have not recognized that slime molds were related to fungi even when phylogeny was based only on morphological evidence.
Although there was already a great deal of evidence indicating that the flagellate fungi were polyphyletic, molecular techniques now also demonstrated that some groups were very distantly related to the fungi. Recall that on page 63, Figure 3-2 of your text showed a tree, which was based primarily on rDNA sequence analysis:
This tree indicates that the Chytridiomycota should be classified in the Kingdom Myceteae, with the fungi, the Oomycota should be in the Kingdom Stramenopila with the Chrysophyta and Phaeophyta as proposed by Pringsheim (1858) and Kriesel (1969). Although their theory did turned out to agree with this modern interpretation in phylogeny, they based their classification of the Oomycota only on superficial morphological similarities. The Hyphochytriomycota were also first classified in this group at this time. The different phyla of slime molds are also shown here to be more distantly related than once believed. Also, note that the Rhodophyta is unrelated to the Ascomycota.
Although phylogeny in the higher taxa of fungi seem to be more resolved, the lower taxa now seem to be more confused. DNA sequence analysis do not support the Dipodascopsis-like hypothetical ancestor that was once thought to link the Zycomycota to the Ascomycota. Thus, we no longer have a link between the two phyla. Another Ascomycota dogma that has been demonstrated to be incorrect is the monophyletic origin of the ascosporogenous yeasts. Members of Saccharomycetales no longer appear to be monophyletic and are more distantly related to other ascosporogenous yeasts.
Phylogeny within the Basidiomycota has also become more confused. The relatedness of taxa within this phylum, based on the morphology of the basidium, which was the main character used to classify fungi in this phylum, is not in agreement with DNA sequence analysis. Instead, it appears that the septal pore apparatus is a better indicator of relationship between members of the Basidiomycota. Thus, with the exception of the Tremellales, all of the various basidial types, that are formed in basidiocarps now appear to be more closely related than once believed, i.e. Agaricales, Gasteromycetes, Auriculariales, Dacrymycetales, etc. are now believed to form a monophyletic group with the Tremellales as a sister group. The Ustilaginomyetes and Uredinomycetes are believed to be more distantly related.
Compare the above treatment of the Basidiomycota with one classification scheme, below, based on basidial morphology:
Class: Homobasidiomycetes - Basidium typically clavate, unicellular with four sterigmata. Basidiocarp always present.
Class: Heterobasidiomycetes - Basidium morphology variable, not usually clavate and unicellular. Basidiocarp present or not. This group includes the Uredinales, Ustilaginales, Tremellales, Auriculariales, Dacrymycetales, etc.
Literature Cited
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