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New Views on Fungal Evolution Based on DNA Markers and the Fossil Record

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New Views on Fungal Evolution Based on DNA Markers and the Fossil Record Research in Microbiology 153 (2002) 125–130 www.elsevier.com/locate/resmic Mini-review New views on fungal evolution based on DNA markers and the fossil record Dirk Redecker Institute of Botany, Hebelstrasse 1, University of Basel, 4056 Basel, Switzerland Received 24 October 2001; accepted 23 November 2001 First published online 14 February 2002 Abstract Molecular markers have facilitated a better understanding of the evolution of fungi. Molecular phylogenetics determined the closest relatives of fungi and defined natural groups within the true fungi. The impact of molecular markers on the population biology of fungi has been enormous, helping to define cryptic species and elucidating fungal breeding biology. The interaction between molecular phylogenetics and the fungal fossil record is discussed. 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Fungi; Evolution; Molecular phylogeny; Population biology 1. Introduction the symbiosis between fungi and Ambrosia beetles, which have special pouches to carry their fungal symbionts [1]. Fungi have traditionally been defined as a group of eu- Even ruminants are among the symbiotic partners of fungi, karyotic, achlorophyllous organisms with adsorptive nutri- harboring chytrid fungi in their digestive tract. tion and filamentous somatic structures, known as “hyphae” Morphological characteristics at the macroscopic and the or “mycelium” [1]. It has become clear that several phylo- light microscopic level that can be used for classification are genetically unrelated eukaryotic lineages fall within this dis- often scarce in fungi. Therefore, views of their evolutionary parate array of organisms traditionally studied by mycolo- relationships have been obscured by convergence and homo- gists. One lineage is known as the true fungi [7], comprising plasy in many cases. With the advent of electron microscopy, the fungi forming macroscopic fruiting structures and many a wealth of more useful characters became available, but in others. This group is monophyletic, i.e., it contains all the many cases these were still problematic to interpret phylo- descendants of one common ancestor. genetically. In the past few years, phylogenetic analyses of Fungi are found in all ecosystems and show a great DNA sequences have offered the opportunity to elucidate diversity of lifestyles. It has been estimated there may be as fungal phylogeny without the need to interpret phenotypic many as 1.5 million species of true fungi, but only 69 000 characters and provided numerous new insights into fungal have been described so far [13]. They live as saprobes, evolution. Recent fossil findings of fungi allowed a better decaying dead organic material, or in symbiosis with other understanding of the evolutionary history of fungi. Fossil organisms. Symbiotic interactions range from parasitism, record and molecular data continue to complement and chal- as exemplified by the huge variety of fungal diseases, lenge each other. to mutualistic interactions, benefiting both partners. Plants are the symbiotic partners in the mycorrhizal interactions. Green algae and cyanobacteria participate in the lichen 2. What is a fungus? symbiosis. Insects form many different kinds of fungal symbioses. Examples are the fungus gardens of attine With the rise of molecular phylogenetics, fungi sensu ants, Trichomycetes lining the inside of insect guts or stricto (the true fungi) were defined as a monophyletic group [7]. This group comprised Basidiomycota, Ascomy- E-mail address: [email protected] (D. Redecker). cota, Zygomycota and Chytridiomycota. 0923-2508/02/$ – see front matter 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII:S0923-2508(02)01297-4 126 D. Redecker / Research in Microbiology 153 (2002) 125–130 Based on biochemical and ultrastructural characters it the establishment of the mitochondrial endosymbiosis. How- had already been clear that several groups traditionally ever, most protein genes, among them tubulins, placed the treated as fungi sensu lato are not a part of the true Microsporidia within the fungi [20], although it was not pos- fungi [1]. DNA sequence data have made it possible to sible to determine their closest relatives. These findings in- place these groups in other major eukaryotic clades defined dicate that an extremely increased mutation rate in the ri- by molecular phylogenetics, where this was not already bosomal genes caused the artifact of phylogenetic analysis possible by morphological analyses. known as long branch attraction, resulting in a basal place- The Oomycota, for instance, are members of the Stra- ment of this group within the eukaryotes. The discordant re- menopila clade, although they resemble the true fungi sults highlight possible problems that can arise when study- closely in their growth form, their adsorptive and parasitic ing major eukaryotic lineages with single-gene phylogenies. lifestyles and the formation of spores. The Stramenopila are Ribosomal DNA is still the gold standard of phylogenetic a major eukaryotic lineage comprising brown algae, diatoms analysis and will continue to be so, but to elucidate the re- and chrysophytes [26]. Some members of the Oomycota are lationships among major eukaryotic clades it is necessary known as “water molds”, some are prominent pathogens, to employ alternative phylogenetic markers (e.g., elongation e.g., Phytophthora or Peronospora. The Oomycetes are a factor alpha, tubulins, actin). fascinating example of convergence to the true fungi. These two groups of organisms adapted a similar lifestyle although they are not related at all and evolved independently. Inter- 3. Many fungal lifestyles and morphologies arose estingly, no mutualistic symbioses resembling mycorrhizae several times (and were lost again) and lichens are known from this group. It will be interesting in the future to compare the cell biology of true fungi and Molecular phylogenetics showed that phylogenetic re- Oomycota to find the reason for this apparent difference. lationships of the “lower fungi” (Zygomycota/Chytridio- There is now compelling evidence that the closest known mycota) are generally more complicated than previously relatives of the true fungi are animals [2], and not green thought. Zygomycota have a non-septate mycelium and dur- plants, in spite of the historically-grounded responsibility of ing sexual reproduction they form typical structures known botanists for fungi. The sister group relationship of animals as zygospores. The Chytridiomycota are characterized by and fungi is supported by phylogenetic analysis of several motile reproductive cells that have a single, posteriorly di- independent genes and by a characteristic insertion in the rected flagellum. They are thought to be the most ancient elongation factor alpha gene [2]. It can be speculated that fungal group, because they retained this and other features both groups arose from one-celled heterotrophic organisms characteristic of life in the water [1]. Occasionally, the similar to another group that forms a monophyletic clade Chytridiomycota were placed in the protists but molecular with animals and fungi, the choanoflagellates. These resem- phylogenetics confirmed that they are true fungi [7]. ble both the earliest branch of animals, the sponges, and the However, there is some evidence that both Zygomy- earliest branch of the true fungi, the chytrids [3]. cota and Chytridiomycota are not monophyletic [18]. Both Another recently defined group of organisms branching comprise several diverse lineages which are only distantly close to the animal-fungal divergence are the Ichthyosporea, related. Molecular phylogenetics of the Zygomycota and an enigmatic group comprising parasites of marine animals. Chytridiomycota has not been without problems because of Initially, they were informally named “DRIPs” after the the ancient age of the clades and the drastically increased first known members of this group (Dermocystidium,the mutation rates in the ribosomal RNA of some Zygomycota “Rosette agent”, Ichthyophonus,andPsorospermium) [27]. lineages. These lineages cause very long branches in phy- Since that first study, a number of additional members logenetic trees and their placement tends to be problematic. of the group have been discovered, and the group was Therefore it may be misleading to rely on rRNA alone to named Ichthyosporea [9]. Some of these parasites have elucidate the relationship of the deep branches within the fungus-like thalli and sporangia. That is also the case for true fungi. A comprehensive analysis of Zygomycota and Amoebidium parasiticum, which was most recently reported Chytridiomycota, using multiple genes, remains to be done, as a member of the Ichthyosporea [4]. Amoebidium was but studies of subgroups of these phyla yielded interesting previously thought to be a Trichomycete (Zygomycota), results. based on its habitat as arthropod symbiont and the thallus In the Zygomycota, the Mucorales, a group of ubiquitous morphology. saprophytes, have been studied using a combination of se- Hardly any problem case of molecular phylogenetics can quence data from small and large subunit rDNA and elonga- be imagined to be as controversial as the Microsporidia. tion factor alpha [25]. The striking result was that most of the This enigmatic group of unicellular intracellular parasites taxa on the family level that were defined by classical mor- was thought to be one of the deepest-branching eukaryotic phological criteria were not monophyletic. Even
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