12 The Fungi John W. Taylor

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Joseph Spatafora

Kerry O’Donnell

Franзois Lutzoni

Timothy James

171

The fungi contain possibly as many as 1.5 million species

(Hawksworth 1991, 2001), ranging from organisms that are

microscopic and unicellular to multicellular colonies that can

be as large as the largest animals and plants (Alexopoulos

et al. 1996). Phylogenetic analyses of nuclear small subunit

(nSSU) ribosomal DNA (rDNA) put fungi and animals as

sister clades that diverged 0.9 to 1.6 billion years ago

(Wainright et al. 1993, Berbee and Taylor 2001, Heckman

et al. 2001). The grouping of fungi and animals as sister taxa

is controversial, with some protein-coding genes supporting

the association and others not (Wang et al. 1999, Loytynoja

and Milinkovitch 2001, Lang et al. 2002). Assuming that

fungi and animals are sister taxa, a comparison of basal fungi

(Chytridiomycota) with basal animals and associated groups

(e.g., choanoflagellates and mesomycetozoa) should shed

light on the nature of the last common ancestor of animals

and fungi (fig. 12.1). It must have been unicellular and motile,

indicating that multicellularity evolved independently

in the two clades, and again in the several differently pigmented

plant clades (M. Medina, A. C. Collins, J. W. Taylor,

J. W. Valentine, J. H. Lips, L. Amaral-Zettler, and M. L. Sogin,

unpubl. obs.). Fungi, like animals, are heterotrophs but,

unlike animals, fungi live in their food. They do so as unicellular

yeasts or as thin, filamentous tubes, termed hyphae

(hypha, singular), which absorb simple molecules and export

hydrolytic enzymes to make more simple molecules out

of complex polymers, such as carbohydrates, lipids, proteins,

and nucleic acids. Fungi have been spectacularly successful

in the full range of heterotrophic interactions—decomposition,

symbiosis, and parasitism. Fungi are well known to

decay food stored too long in the refrigerator, wood in homes

that have leaky roofs, and even jet fuel in tanks where condensation

has accumulated. In nature, apart from fire, almost

all biological carbon is recycled by microbes. The hyphae of

filamentous fungi do the hard work in cooler climes and

wherever invasive action is needed, as in the decay of wood.

Fungi enter into many symbioses, three of the most widespread

and enduring are with microbial algae and cyanobacteria

as lichens, with plants as mycorrhizae, and again with

plants as endophytes. These symbioses are anything but rare.

Nearly one-fourth of all described fungi form lichens, and

lichens are the last complex life forms seen as one travels to

either geographic pole (Brodo et al. 2001). Almost all plant

species form mycorrhizae, and there is good fossil and molecular

phylogenetic evidence that the first land plants got

there with fungi in their rhizomes (Smith and Read 1997).

There probably is not a plant that lacks a fungal endophyte,

and there is good evidence that the endophytes improve plant

fitness by deterring insect and mammalian herbivores and

affect plant community structure (Clay 2001). Fungi are not

limited to symbioses with autotrophs. Symbioses with animals

are also prevalent, with partners ranging from ants and

other insects to the gut of many ruminate animals and other

herbivores (Blackwell 2000). Many insects may have been

able to occupy new habitats due to associations with gut

yeasts that provide digestive enzymes (Suh et al. 2003).

David S. Hibbett

David Geiser

Thomas D. Bruns

Meredith Blackwell

172 The Relationships of Fungi

Fungi also are well-known parasites. The stories of the spread

of plant pathogens such as wheat rust, chestnut blight, and

Dutch elm disease are biological and social tragedies, often

initiated by intercontinental transport of pathogenic fungi

(Agrios 1997). Fungi also plague humans, with athlete’s foot

and ringworm being the relatively benign end of a spectrum

that ends in coccidioidomycosis, histoplasmosis, and other

systemic and sometimes fatal diseases (Kwon-Chung and

Bennett 1992). In the era of immune suppression, many

yeasts and filamentous fungi, heretofore considered not to

be serious human pathogens, have been found to cause grave

systemic disease, among them Aspergillus fumigatus and Candida

albicans. The close relationship of fungi and animals

brings with it a similarity in metabolism that has made it

difficult to find pharmaceuticals that attack the fungus and

not the host.

Fungi have life histories that are far more interesting than

those of most animals. Typically, fungi can mate and use

meiosis to make progeny that have recombined genotypes,

and they also can reproduce clonally via mitosis to make

progeny with identical genotypes (Alexopoulos et al. 1996).

Reproduction involves spore formation, with both mitotic

and meiotic spores often facilitating long-distance transport

and resistance to adverse environmental conditions. Huge

numbers of spores can be produced, with the record annual

spore release of several trillion being held by giant puffballs

and the large fruiting bodies of wood-rotting Basidiomycota.

Reproduction often is triggered by exhaustion of the food

supply. Before mating, individuals find partners by chemical

communication via pheromones, which range from complex

organic compounds in Chytridiomycota and Zygomycota to

oligopeptides in Ascomycota and Basidiomycota. Spores germinate

to produce hyphae or germinate by budding to produce

yeasts; in both cases the cell wall is composed of glucose

polymers, the best known being chitin, a polymer of N-acetylglucosamine.

Most fungi are not self-motile, the exception

being the Chytridiomycota, which produce unicellular

zoospores that have one typical eukaryotic flagellum inserted

posteriorly.

Humans have domesticated yeasts to make bread, beer,

wine, and fermentations destined for distillation. They have

done the same with a number of filamentous fungal species,

with species of Penicillium being the best known because of

their role in making the camembert and roquefort families of

cheese, dry-cured sausage, and the life-saving antibiotic penicillin.

Biologists also have exploited several fungi as model

organisms for genetics, biochemistry, and molecular biology,

among them, Neurospora crassa, Saccharomyces cerevisiae, and

Schizosaccharomyces pombe—Nobel Prize winners all.

Within the monophyletic Fungi, four major groups generally

are recognized: Chytridiomycota, Zygomycota, Basidiomycota,

and Ascomycota (fig. 12.2). Analysis of nSSU rDNA

shows the Ascomycota and Basidiomycota to be monophyletic,

but the Zygomycota and Chytridiomycota are not easily

made into monophyletic groups, and their monophyly,

or lack thereof, is controversial (Nagahama et al. 1995). The

earliest divergences within Fungi involve certain Chytridiomycota

and Zygomycota. The hyphae of these fungi typically

lack the regularly spaced, cross walls (septa) typical of

Ascomycota and Basidiomycota. In Chytridiomycota and

Zygomycota, haploid nuclei are brought together by mating

and fuse without delay. One of the clades radiating among

the Chytridiomycota and Zygomycota leads to the Glomales

+ Ascomycota + Basidiomycota clade. Again, the placement

of the Glomales on this branch may be controversial (James

et al. 2000). Together, the Ascomycota and Basidiomycota

form an informal group, the dikaryomycetes, which have

regularly spaced cross walls in their hyphae, oligopeptide

mating pheromones, and, because of an extended period

between mating and nuclear fusion, pairs of genetically dissimilar

nuclei in mated hyphae (i.e., a dikaryon). In the following

sections, each of these groups is discussed, beginning

with the largest and most familiar ones: Ascomycota,

Basidiomycota, Zygomycota, and Chytridiomycota. Mycologists

study more organisms than are found in the monophyletic

Fungi, but inclusion of these organisms is beyond the

scope of this chapter; some are covered elsewhere in this

volume and are treated in mycology textbooks (Alexopoulos

et al. 1996). These “fungal” groups include the water molds

(Oomycota, Straminipila), home of the infamous plant pathogen

Phytophthora infestans, cause of late blight of potato; the

cellular slime molds (Dictyosteliomycota), home of the model

social microbe Dictyostelium discoideum; the plasmodial slime

molds (Myxomycota), home of the cell biology model organism

Physarum polycephalum; and a myriad of other myxomycetes

having beautiful sporangia. Conversely, some

organisms not presently classified as Fungi may belong there,

especially the microsporidia, a group of obligate animal parasites

that branch deeply on the eukaryote branch in rDNA

trees, but close to, or within, the fungi in some protein gene

trees (Keeling et al. 2000, Tanabe et al. 2002).

Ascomycota

The Acomycota, or sac fungi (Gr. ascus, sac; mycetos, fungi),

are the largest of the four major groups of Fungi in terms

of number of taxa. With approximately 45,000 sexual and

Figure 12.1. Phylogenetic tree showing relationships of the

fungi, animals, and green plants based on nSSU rDNA.

The Fungi 173

asexual species, it accounts for about 65% of all described

fungi (Hawksworth et al. 1995, Kirk et al. 2001). This group

is characterized by the production of meiospores (ascospores)

within sac-shaped cells (asci). It includes more than 98% of

the fungi that combine with green algae or cyanobacteria or

both to form lichens, as well as the majority of fungi that lack

morphological evidence of sexual reproduction (mitosporic

fungi). Ascomycota include many well-known fungi that have

transformed civilization through food and medicine and that

serve as model organisms through which major advancements

in science have been made (Taylor et al. 1993). Some

examples of these fungi include Saccharomyces cerevisiae (the

yeast of commerce and foundation of the baking and brewing

industries, not to mention molecular genetics), Penicillium

chrysogenum (producer of the antibiotic penicillin),

Tolypocladium inflatum (producer of the immunosuppressant

drug cyclosporin A, which revolutionized the field of organ

transplantation), Morchella esculenta (the edible morel), and

Neurospora crassa (the “one-gene-one-enzyme” organism).

There are also many notorious members of Ascomycota that

cause disease in humans and in many ecologically and economically

important organisms. Some of these examples

include Aspergillus flavus (producer of aflatoxin, the fungal

contaminant of nuts and stored grain that is both a toxin and

the most potent known natural carcinogen), Candida albicans

(cause of thrush, diaper rash, and vaginitis), Pneumocystis

carinii (cause of a pneumonia in people with compromised

immune systems), Magnaporthe grisea (cause of rice blast

disease), and Cryphonectria parasitica (responsible for

the demise of 4 billion chestnut trees in the eastern United

States; Alexopoulos et al. 1996).

Characteristics

The shared derived character state that defines members of

the Ascomycota is the ascus (fig. 12.3). It is within the ascus

that nuclear fusion (karyogamy) and meiosis ultimately take

place. In the ascus, one round of mitosis typically follows

meiosis to produce eight nuclei, and eventually eight ascospores;

however, numerous exceptions exist that result in

asci containing from one to more than 100 ascospores, depending

on the species. Ascospores are formed within the

ascus by the enveloping membrane system, a second shared

derived character unique to Ascomycota. This double membrane

system packages each nucleus with its adjacent cytoplasm

and organelles and provides the site for ascospore wall

formation. These membranes apparently are derived from the

ascus plasma membrane in the majority of filamentous species,

and the nuclear membrane in the majority of “true yeasts,”

and are assumed to be homologous (Wu and Kimbrough

1992, Raju 1992).

Within Ascomycota, two major growth forms exist. Species

that form a mycelium consist of filamentous, often

branching, hyphae. Hyphae exhibit apical growth and in

Ascomycota are compartmentalized by evenly spaced septations

that originate by centripetal growth from the cell wall.

These septations are relatively simple in morphology and

possess a single pore through which cytoplasmic connectivity

may exist between hyphal compartments. Numerous examples

exist, however, in which the pores become plugged,

preventing or at least regulating movement between adjacent

hyphal compartments. Hyphae also are the basic “cellular”

building blocks for the different types of fungal tissues (e.g.,

the meiosporangia or fruiting bodies termed ascomata). The

second major type of growth form found within Ascomycota

is the yeast, a single-celled growth form that multiplies most

commonly by budding. Both yeasts and hyphae have cell

walls made of varying proportions of chitin and b-glucans

(Wessels 1994). It is important to note that neither the hyphal

(filamentous) morphology nor the yeast morphology is

indicative of phylogenetic relationships. In fact, many spe-

Figure 12.2. Alternative phylogenetic trees showing the

relationships among the major groups of fungi. Each branch is

monophyletic if flagella have been lost just once in the evolution

of fungi, but both Zygomycota and Chytridiomycota are nonmonophyletic

if flagella have been lost independently.

174 The Relationships of Fungi

cies of Ascomycota are dimorphic, producing both hyphal

and yeast stages at certain points in their life cycle. Regardless

of the growth form, all members of Ascomycota are eukaryotes,

typically possessing a single haploid nucleus, or

several identical haploid nuclei, per hyphal compartment

or yeast cell, although examples exist of diploid species of

Ascomycota (e.g., Candida albicans) or species possessing

long-lived diploid stages (e.g., Saccharomyces cerevisiae).

Reproduction and Life Cycle

Like much of life apart from the vertebrates, fungi have more

than one reproductive option, a phenomenon termed pleomorphy

(Sugiyama 1987). This phenomenon is arguably

most pronounced among members of Ascomycota. The textbook

Ascomycota example can make spores sexually (ascospores

or meiospores) and asexually (conidia or mitospores;

fig. 12.4), although many species are known to reproduce

only by ascospores, and many more are known to reproduce

only by conidia. After meiosis, the ascospores take shape

inside the ascus with new cell walls synthesized de novo in

association with the aforementioned enveloping membrane

system. Conidia contain mitotic nuclei, and their cell wall is

a modification or extension of a preexisting hyphal or yeast

wall. In hyphal Ascomycota, conidia may be produced by

specialized hyphae that range from structures scarcely differentiated

from vegetative mycelium (Geotrichum candidum)

to hyphae consisting of elaborate heads of ornamented

condida (Aspergillus niger; Cole and Kendrick 1981). Classification

of Ascomycota is based on characteristics of sexual

reproduction (i.e., ascomata and asci), and for this reason

species that reproduce only asexually have been problematic

in their integration into the classification of Ascomycota.

In older systems of classification, all asexual members of

Figure 12.3. Macroscopic and microscopic images of meiotic and mitotic stages of Ascomycota. (A)

Young asci and ascospores of Otidea (courtesy of J. W. Spatafora). (B) Scanning electron micrograph

of conidia and conidiophores of Aspergillus (courtesy of C. W. Mims). (C) Lichen thallus of Usnea

showing apothecia (courtesy of S. Sharnoff). (D) Perithecia of Nectria (courtesy of J. W. Spatafora).

(E) Dungscape showing perithecial necks of Sphaeronaemella fimicola emerging from dung substrate

(courtesy of D. Malloch and M. Blackwell). (F) Cross section of cleistothecium of Talaromyces with

asci dispersed throughout central cavity of cleistothecium (courtesy of T. Volk). (G) Kathistes

calyculata perithecium with basal asci and terminal, incurved setae (courtesy of D. Malloch and

M. Blackwell). (H) Ear-shaped apothecia of Otidea (courtesy of W. Colgan III). (I) Cross section of

Lobaria thallus showing arrangement of green algal layer (courtesy of S. Sharnoff). (J) Scanning

electron micrograph of cleistothecium of Uncinula with hooked appendages (courtesy of C. W. Mims).

The Fungi 175

Ascomycota were placed in the admittedly artificial Deuteromycota.

This classification scheme has since been abandoned,

and with the advent of molecular phylogenetics,

sexual and asexual taxa can be integrated into a common system

of classification based on comparison of gene sequences

that are ubiquitously distributed across their genomes (Taylor

1995).

Ascospores and conidia are propagules whose main functions

are dispersal to and colonization of appropriate substrates

or hosts. Ascospores may or may not be forcibly

ejected from an ascus. With forcible ejection, turgor pressure

builds within the ascus, resulting in the eventual violent

eruption of the ascospores from the ascus. In these

systems, wind is the primary dispersal agent. Other members

of Ascomycota do not forcibly eject their ascospores. In

these systems the ascus wall breaks down, passively releasing

the ascospores into the environment. This latter mechanism

is especially common among Ascomycota that rely on

arthropods and water to disperse their ascospores (Ingold

1965). In an analogous manner, conidia also may be produced

in a relatively dry mass and be dispersed by wind, or

may be produced in wet or sticky heads and be dispersed by

water or arthropods (fig. 12.3). In most species, both ascospores

and conidia are capable of germination, restoring

the dominant haploid mycelial stage (fig. 12.4).

Species of Ascomycota may be either self-fertile (homothallic)

or self-sterile (heterothallic), with the latter form

requiring a separate and mating-compatible partner for

sexual reproduction. Genetic regulation of sex expression

and mating is well understood in several model members

of Ascomycota, such as budding yeast (Saccharomyces cerevisiae),

fission yeast (Schizosaccharomyces pombe), and Neurospora

crassa; there are two sexes, and mating is coordinated

by the aforementioned oligopeptide pheromones (Marsh

1991, Glass and Lorimer 1991). In yeast species, individual

yeast cells function as gametangia and fuse to form the zygote,

which eventually becomes the ascus after karyogamy

and meiosis. In hyphal species, female gametangia (ascogonia)

are produced and are fertilized either by male gametangia

(antheridia) or by minute conidia that function as

spermatia. In this latter example, cytoplasmic fusion (plasmogamy)

may not be immediately followed by karyogamy,

leading to a short phase where two genetically different nuclei

occupy the same hyphal segment, as mentioned in the

introductory remarks. These dikaryotic hyphae may be protected

and nourished by differentiated haploid hyphae,

which form a fruiting body (the ascoma; plural, ascomata;

fig. 12.3). It is within the ascomata that asci eventually are

produced from the dikaryotic hyphae originating from sexual

reproduction. Asci exhibit a range of morphologies across

Ascomycota with unitunicate asci possessing a single functional

wall layer and bitunicate asci possessing two functional

wall layers that operate much like a “jack-in-the-box” (Luttrell

1951, 1955). Unitunicate asci may be operculate and possess

an apical lid (operculum) through which ascospores are

released, or they may be inoperculate and release their ascospores

through an apical pore or slit. As discussed below,

ascus morphology does correlate with phylogeny. Ascospores

are released from the asci as described above and germinate

to form a new haploid mycelium, which will go on to produce

hyphae, conidia, and ascospores that are characteristic

of the species.

Nutrition, Symbioses, and Distribution

Like other fungi, members of Ascomycota are heterotrophs

and obtain nutrients from dead (saprotrophism) or living

(ranging from mutualism through parasitism) organisms

(Griffin 1994, Carroll and Wicklow 1992). If water is present,

as saprotrophs they can consume almost any carbonaceous

substrate, including jet fuel (Amorphotheca resinae) and wall

paint (Aureobasidium pullulans), and play their biggest role

in recycling dead plant material. As symbionts, they may form

obligate mutualistic associations with photoautotrophs such

as algae and cyanobacteria (lichens; Brodo et al. 2001,

Lutzoni et al. 2001, Nash 1996; fig. 12.3), plant roots (mycorrhizae;

Varma and Hock 1999), and the leaves and stems

of plants (endophytes; Arnold et al. 2001, Carroll 1988,

1995). Other Ascomycota form symbiotic associations with

an array of arthropods, where they can line beetle galleries

and provide nutrition for the developing larvae (Ceratocystis

and Ophiostoma) or inhabit the gut of insects to participate

in sterol and nitrogen metabolism (Symbiotaphrina and other

yeasts and yeastlike symbionts). In return, the insects maintain

pure cultures of the fungi and provide for their trans-

Figure 12.4. Generalized Ascomycota life cycle. The thallus

(body) typically is hyphal and haploid. Vegetative hyphae can

differentiate into reproductive structures for clonal (conidiophores,

conidia) or sexual reproduction (spermatia, gametangia)

or both. Sexual reproduction involves mating to produce, in a

limited set of hyphae, a short-lived dikaryotic phase (N+N).

Typically, the dikaryon is surrounded by a developing haploid

ascoma. Karyogamy produces a zygote and is followed immediately

by meiosis to produce ascospores. Both ascospores and

conidia germinate to produce haploid hyphae.

176 The Relationships of Fungi

port (Benjamin et al. in press, Currie et al. 2003). As parasites

and pathogens, ascomycetes account for most of the

animal and plant pathogenic fungi, including those mentioned

in the introduction to the Ascomycota section and

many others, such as Ophiostoma ulmi, the Dutch elm disease

fungus that is responsible for the demise of elm trees in

North America and Europe (Agrios 1997). Numerous species

are known from marine and aquatic ecosystems, where

they are most frequently encountered on plant debris but

may also be parasites of algae and other marine organisms

(Kohlmeyer and Kohlmeyer 1979, Spatafora et al. 1998).

Ascomycota can be found on all continents and many

genera and species display a cosmopolitan distribution (Candida

albicans or Aspergillus flavus). Others are found on more

than one continent (Ophiostoma ulmi or Cryphonectria parasitica),

but many are known from only one narrowly restricted

location. For example, the white piedmont truffle (Tuber magnatum)

is known from only one province of northern Italy.

Relationships of Ascomycota to Other Fungi

The Ascomycota are the sister group to Basidiomycota. This

relationship is supported by the aforementioned presence in

members of both groups of regularly septate hyphae, and

pairs of unfused haploid nuclei present in some stage of the

thallus after mating and before nuclear fusion (dikaryons).

Further support comes from the apparent homology between

structures that coordinate simultaneous mitosis of dikaryotic

nuclei (Ascomycota croziers and Basidiomycota clamp connections).

Finally, numerous molecular phylogenetic studies

all support the hypothesis that Ascomycota and Basidiomycota

share a more recent common ancestor with one another

than with any other major group (e.g., Zygomycota,

Chytridiomycota) in Fungi (e.g., Bruns et al. 1992, Berbee

and Taylor 1993, Tehler et al. 2000).

Phylogenetic Relationships within Ascomycota

Comparison of the genes that encode for the nuclear ribosomal

RNAs (rRNAs) and the gene family of RNA polymerase,

especially RNA polymerase II subunit B, supports

a monophyletic Ascomycota that possesses three major subgroups

(fig. 12.5; Berbee and Taylor 1993, Bruns et al. 1992,

Spatafora 1995, Liu et al. 1999, Lutzoni et al. 2001). In

the most recent classification (Eriksson et al. 2003), the

three groups are designated subphylum Taphrinomycotina

(= class Archiascomycetes), subphylum Saccharomycotina

(= class Hemiascomycetes), and subphylum

Pezizomycotina (= class Euascomycetes).

Taphrinomycotina are a group recently discovered from

comparison of nucleic acid sequences and contains several

species previously thought to be Saccharomycotina (Nishida

and Sugiyama 1994). Some species, such as the fission yeast,

Schizosaccharomyces pombe, are unicellular, but others grow

as hyphae as well as single cells (e.g., Taphrina species).

Members of Taphrinomycotina do not produce ascomata

with the exception of the genus Neolecta. Neolecta produces

stipitate, club-shaped ascomata and once was classified

among the Pezizomycotina. Recent molecular phylogenetic

studies of independent gene data sets do not support the

placement of Neolecta within the Pezizomycotina (Landvik

1996, Landvik et al. 2001). Rather all are consistent with its

placement in the Taphrinomycotina, suggesting that the

ability to form ascomata arose early in the evolution of

Ascomycota. Monophyly of the Taphrinomycotina is not

strongly supported by current analyses, however, and it is

possible that the genera in question arose independently,

possibly during the early radiation of Ascomycota.

Saccharomycotina consist of organisms most biologists

recognize as yeasts or “true yeasts” and is home to one of the

best-known species of fungi, Saccharomyces cerevisiae, better

known as the baker’s yeast. Although most Saccharomycotina

are primarily unicellular, numerous species do make

abundant hyphae, but none produce ascoma (Barnett et al.

1990). Phylogenies within the Saccharomycotina are among

the most developed in the fungi because the taxon sampling

is very dense (Kurtzman and Robnett 2003).

Pezizomycotina contain well more than 90% of the members

of Ascomycota. Most species exhibit a dominant hyphal

growth form, with almost all of the sexually reproducing

forms possessing ascomata. Members of Pezizomycotina fall

into two major categories: ascohymenial, which form after

the initial sexual fertilization event, and ascolocular, which

form before the initial sexual fertilization event. Ascohymenial

ascomata may be closed (cleistothecium), open by a narrow

orifice (perithecium), or broadly open like a cup (apothecium;

see fig. 12.3). They may be less than a millimeter in

diameter in the case of perithecia and cleistothecia, or up to

10 cm in diameter in the case of some apothecia. The common

names often used to denote groups possessing ascohymenial

ascomata include “plectomycetes” for the cleistothecial

species, “pyrenomycetes” for the “perithecial” species, and

“discomycetes” for the apothecial species. The ascolocular

ascomata are referred to as ascostromata, and the common

name given to these fungi is the “loculoascomycetes.” Most

current phylogenetic hypotheses propose that the apothecium

(discomycetes in fig. 12.5) is the most primitive ascomatal

morphology within the Pezizomycotina (Gernandt et al.

2001, Eriksson et al. 2003) and that the remaining ascomatal

morphologies are more derived, in some cases

through numerous independent events of convergent and

parallel evolution (fig. 12.5, Berbee and Taylor 1992,

Spatafora and Blackwell 1994, Suh and Blackwell 1999,

Lutzoni et al. 2001). Pezizomycotina contain species of all

ecologies, including plant pathogens (e.g., Pyrenophora

tritici-repentis), animal pathogens (e.g., Cordyceps militaris),

mycorrhizae (e.g., Tuber melanosporum), endophytes (e.g.,

Rhytisma acerinum), and innumerable plant decay fungi. Importantly,

Pezizomycotina include more than 98% of fungi

that are lichenized. Lichenized fungi are an amazingly sucThe

Fungi 177

cessful group, accounting for approximately 42% of all described

species of Ascomycota and probably close to 50% of

the known members of Pezizomycotina. Lichens are ecologically

important organisms that cover as much as 8% of Earth’s

land surface, serve as important food sources for animals in

harsh arctic environments, and function as pollution indicators

in industrialized parts of the world. Lichens were

widely believed to have arisen independently multiple

times, accounting for the high diversity and mixed occurrence

of lichenized and nonlichenized fungal species within

Ascomycota (Gargas et al. 1995). A recent comparative phylogenetic

study reported that lichens may have evolved earlier

than previously believed within Pezizomycotina, and that

independent gains of lichenization have occurred one to three

times during Ascomycota evolution but have been followed

by multiple independent losses of the lichen symbiosis

Figure 12.5. Depiction of the current understanding of relationships among members of Ascomycota,

sister group to the Basidiomycota (adapted from Suh and Blackwell 1999, Bhattacharya et al.

2000, Platt and Spatafora 2000, Gernandt et al. 2001, Kirk et al. 2001, Lutzoni et al. 2001,

McLaughlin et al. 2001, Kauff and Lutzoni 2002). Higher taxa of Eriksson et al. (2003) and

“common names” are shown on the tree before and after “/,” respectively. Taxa listed at the tips of

terminal branches that include lichen-forming species are denoted “(L).” Note the phylogenetic

uncertainty among several groups, including Taphrinomycotina (= Archiascomycetes) and within

the Pezizomycotina (= Euascomycetes). Common groups such as the “inoperculate discomycetes”

(e.g., Orbiliomycetes, Leotiomycetes, Lecanoromycetidae, and Ostropomycetidae) and “loculoascomycetes”

(e.g., Chaetothyriales, Dothideomycetidae, Verrucariales, and Pyrenulales) do not

denote monophyletic groupings. Most cleistothecial fungi (“plectomycetes”) occur in a monophyletic

group (Ascospheriales, Eurotiales, Onygenales; Geiser and LoBuglio 2001), whereas others are

derived members of other groups such as the Sordariomycetes (“pyrenomycetes”). The vast majority

of “pyrenomycetes” are members of Sordariomycetes, with a few unique and poorly known

perithecial species among Laboulbeniomycetes (Weir and Blackwell 2001). The Lecanoromycetes, a

recently established group of mostly lichen-forming species, include four major subgroups of

Ascomycota: Acarosporomycetidae, Eurotiomycetidae, Lecanoromycetidae, and Ostropomycetidae.

Basidiomycota

Taphrinomycotina /Archiascomycetes 1

Taphrinomycotina/Archiascomycetes 2

Taphrinomycotina /Archiascomycetes 3

Saccharomycotina/Hemiascomycetes

Orbiliomycetes/Inoperculate Discomycetes 1

Pezizomycetes/Operculate Discomycetes

Leotiomycetes/Inoperculate Discomycetes 2

Leotiomycetes/Inoperculate Discomycetes 3

Laboulbeniomycetes /Pyrenomycetes 1

Sordariomycetidae/Pyrenomycetes 2

Dothideomycetidae/ Loculoascomycetes 1 (L?)

Arthoniomycetidae/Inoperculate Discomycetes 4 (L)

Lichinomycetes/Inoperculate Discomycetes 5 (L)

Chaetothyriales, V errucariales/Loculoascomycetes 2 (L)

Pyrenulales/Loculoascomycetes 3 (L)

Ascosphaeriales, E urotiales, O nygenales/Plectomycetes

Acarosporomycetidae/Inoperculate Discomycetes 6 (L)

Lecanoromycetidae/Inoperculate Discomycetes 7 (L)

Ostropomycetidae/Inoperculate Discomycetes 8 (L)

Ascomycota

Pezizomycotina /

Euascomycetes

Sordariomycetes /

Lecanoromycetes /

Eurotiomycetidae /

178 The Relationships of Fungi

(Lutzoni et al. 2001). As a consequence, major Ascomycota

groups of exclusively non-lichen-forming species, which

include the medically important species Exophiala and Penicillium

(e.g., Chaetothyriales and Plectomycetes), would have

been derived from lichen-forming ancestors (fig. 12.5).

Although most of the recent molecular phylogenetic efforts

have been directed at the Pezizomycotina, interrelationships

of the major groups within Pezizomycotina are

still poorly understood and not confidently resolved

by phylogenetic analyses of the current data. Figure 12.5

presents the most current understanding of the relationships

of the major groups within the Pezizomycotina; detailed

discussion is available in Alexopoulos et al. (1996),

Holst-Jensen et al. (1997), Berbee (1998), Liu et al. (1999),

Eriksson et al. (2003), Gernandt et al. (2001), Lutzoni et al.

(2001), and Miadlikowska and Lutzoni (in press), to name

a few.

Basidiomycota

The Basidiomycota (Gr. basidion, small base or pedestal; mykes,

fungi) contain roughly 22,000 described species, which is

approximately 35% of the known species of fungi (Hawksworth

et al. 1995, Kirk et al. 2001). Basidiomycetes include

some of the most familiar and conspicuous of all fungi,

namely, mushrooms and polypores, as well as yeasts (singlecelled

forms) and other relatively obscure taxa. Some basidiomycetes

are economically important edible species,

including button mushrooms (Agaricus bisporus), shiitake

mushrooms (Lentinula edodes), and chanterelles (Cantharellus

cibarius), whereas others are deadly poisonous (e.g., Amanita

phalloides) or hallucinogenic (Psilocybe spp.). The latter play

important roles in traditional shamanic cultures of Central

America (Wasson 1980).

The overwhelming majority of basidiomycetes are terrestrial,

but some species can be found in marine or freshwater

habitats, including many basidiomycete yeasts (Fell et al.

2001). Some basidiomycetes have free-living, saprotrophic

(decomposer) lifestyles, whereas others live in symbiotic associations

with plants, animals, and other fungi. The oldest

fossils of the group are hyphae with diagnostic clamp connections

from the Pennsylvanian period [~290 million years

ago (Mya)], but recent molecular clock estimates suggest that

the common ancestor of all modern basidiomycetes lived at

least 500 Mya, and maybe 1.0 billion years ago (Dennis 1970,

Berbee and Taylor 2001, Heckman et al. 2001).

Tremendous progress has been made in basidiomycete

phylogenetics through the use of molecular characters. Three

major groups are now recognized, the Urediniomycetes,

Ustilaginomycetes, and Hymenomycetes (Swann and Taylor

1995), and the major clades within these groups largely

have been delimited (fig. 12.6). Nevertheless, many aspects

of the relationships within and among the major groups remain

poorly understood.

Characteristics and Life History

The dominant phase of the life cycle in most basidiomycetes

is a heterokaryotic mycelium, which is a network of hyphae,

in which each cell contains two different types of haploid

nuclei resulting from the mating of two monokaryotic (haploid,

uninucleate) mycelia (fig. 12.7). Historically, it has been

very difficult to determine the longevity and spatial distribution

of mycelia, but recently molecular markers have been

used to study this phase of the life cycle—with astonishing

results. In the “honey mushroom,” Armillaria (Hymenomycetes),

mycelia have been discovered that inhabit continuous

patches of forest of many acres. One giant Armillaria

mycelium in a Michigan forest was estimated to be about

1500 years old, with a mass of around 10,000 kg (Smith et al.

1992). Armillaria is a wood-decaying timber pathogen that

forages along the forest floor using rootlike rhizomophs. Most

other basidiomycetes, especially those that colonize patchy,

ephemeral resources (e.g., dung) or that lack rhizomorphs,

probably have much more limited mycelia.

Sexually reproducing basidiomycetes produce cells called

basidia (from which the group derives its name), in which

the two haploid nuclei fuse, immediately undergo meiosis,

and give rise to haploid spores (fig. 12.7). Thus, there is

usually only a single diploid cell in the entire life cycle. In

most species, the spores are discharged from the basidia by

a forcible mechanism termed ballistospory that is unique to

basidiomycetes. Ballistospory has been secondarily lost in

puffballs and their relatives (which produce spores within

enclosed fruit bodies), as well as in aquatic species and

in most smut fungi. Basidia often are produced in elaborate,

multicellular fruiting bodies (the basidioma; plural,

basidiomata), although some species produce basidia directly

from single-celled yeasts. Fruiting bodies are the most visible

stage of the life cycle and encompass an amazing diversity

of forms, including mushrooms, puffballs, bracket fungi,

false truffles, jelly fungi, and others.

Numerous variations on the basic life cycle described

above have evolved in basidiomycetes. In many groups,

asexual spores are produced, from either monokaryotic or

heterokaryotic hyphae, and some basidiomycetes have no

known sexual stage at all (fig. 12.7). Some basidiomycetes

are heteromorphic, alternating between a yeast phase and a

filamentous phase. The most complex life cycles in basidiomycetes

are those of the plant pathogens called rusts

(Urediniomycetes), which have multiple spore-producing

stages that may be formed on two, unrelated plant hosts.

Ecological Importance

Basidiomycetes play diverse ecological roles, but the decay

of wood and other plant tissues may be the single most important

process performed by the group. Although other

fungi, particularly certain groups in the ascomycetes, can

digest cellulose and lignin (the major components of plant

The Fungi 179

cell walls), this ability is best developed in the Hymenomycetes

(Rayner and Boddy 1988, Hibbett and Thorn 2001,

Hibbett and Donoghue 2001). With few exceptions, the

major timber pathogens and saprotrophic wood decayers are

basidiomycetes—this role makes their impact on forest systems

substantial from both ecological and management perspectives

(Edmonds et al. 2000, Rayner and Boddy 1988).

Basidiomycetes use a diverse array of enzymes to digest wood

and plant debris in leaf litter and soil (Cullen 1997, Reid

1995). Because of their enzymatic capabilities, basidiomycetes

have come under scrutiny for possible applications in

bioremediation and biopulping (involved in paper production).

A recent project to sequence the genome of the

wood-decaying basidiomycete Phanerochaete chrysosporium

(Hymenomycetes) was motivated, in part, by the potential

of its enzymes for degrading recalcitrant substrates.

Ectomycorrhizal symbiosis (an association involving

fungal hyphae and the roots of trees) is another major role

that is well developed within the basidiomycetes. Ectomycorrhizal

basidiomycetes have been shown to scavenge

mineral nutrients directly from organic matter, thereby

providing their host trees exclusive access to nutrient pools

Figure 12.6. Phylogenetic relationships, basidia, and fruiting bodies of basidiomycetes. (A)

Phylogenetic relationships of basidiomycetes, based on trees and classifications published by Swann

et al. (2001: fig. 1); Swann and Taylor (1995: figs. 1–2); Bauer et al. (2001: figs. 33, 34); Hibbett

and Thorn (2001: figs. 1F, 2); Fell et al. (2001: fig. 19B); and Wells and Bandoni (2001). Several

minor clades of uncertain placement are not shown. (B–E). Diversity of basidia. (B) Leucosporidium

fellii (Urediniomycetes; after Fell et al. 2001: fig. 3). (C) Tilletia caries (Ustilaginomycetes; after

Oberwinkler 1977: fig. 24). (D) Dacrymyces stillatus (Hymenomycetes; after Wells and Bandoni

2001: fig. 13). (E) Cantharellus cibarius (Hymenomycetes; after Oberwinkler 1977: fig. 28). (F–I)

Diversity of fruiting bodies in the Hymenomycetes. (F) Phlogiotis helvelloides. (G) Amanita species.

(H) Phallus species (primordium on right). (I) Inonotus dryadeus. Drawings by Zheng Wang.

180 The Relationships of Fungi

that are unavailable to most plants (Haselwandter et al. 1990,

Perez-Moreno and Read 2000). In return, ectomycorrhizal

basidiomycetes receive sugars from their plant hosts. More than

6000 species of Hymenomycetes are known or suspected to

be ectomycorrhizal, as well as a handful of ascomycetes and

even zygomycetes (Molina and Trappe 1982, Smith and Read

1997). The plants that are involved in ectomycorrhizal symbioses

include pines, oaks, poplars, chestnuts, birches, dipterocarps,

eucalypts, and caesalpinoid legumes—that is, the

dominant tree species in many temperate and some tropical

forest ecosystems. There is strong evidence that ectomycorrhizal

basidiomycetes have been derived multiple times from saprotrophic

ancestors (Bruns et al. 1998, Gargas et al. 1995), and

some analyses suggest that reversions to saprotrophy also have

occurred (Hibbett et al. 2000).

Plant parasitism is phylogenetically the most widespread

ecological niche within the basidiomycetes. The rusts

(Urediniomycetes), with more than 7000 described species,

are a particularly successful group. Wheat rusts, coffee rust,

and fusiform and blister rust of pines are excellent examples

of species that have a major economic impact on agriculture

and forestry (Edmonds et al. 2000, Swann et al. 2001). Rusts

use angiosperms, gymnosperms, lycopods, and pteridophytes

as hosts, whereas closely related taxa parasitize mosses

and scale insects. The smuts, which comprise a polyphyletic

group composed of members of both the Ustilaginomycetes

and Urediniomycetes (fig. 12.6), are important parasites that

attack a huge diversity of angiosperms. Ustilago and Tilletia

species (e.g., U. hordei, U. tritici, U. maydis, T. caries, and T.

controversa) that occur on cereal crops cause large agricultural

losses. In both the rusts and smuts there is widespread

phylogenetic tracking of hosts, but jumps to unrelated hosts

are well documented (Bauer et al. 2001, Sjamsuridzal et al.

1999, Vogler and Bruns 1998).

Saprotrophy, ectomycorrhizal symbiosis, and plant parasitism

are by no means the only lifestyles represented in basidiomycetes.

Basidiomycetes also parasitize other fungi and

animals—an example is the human parasite Filobasidiella

neoformans, causative agent of cryptococcosis. Basidiomycota

form symbioses with insects, such as bark beetles and the

leaf-cutter ants of the neotropics (Chapela et al. 1994). They

also attack and digest bacteria and microscopic invertebrates,

apparently as a means by which they acquire additional nitrogen

(Barron 1988, Thorn and Barron 1984, Klironomos

and Hart 2001). Basidiomycota also enter into lichenized

symbioses with photosynthetic algae (Gargas et al. 1995,

Lutzoni and Pagel 1997). These examples demonstrate some

of the ecological diversity of basidiomycetes but hide the fact

that we actually know very little about the basic ecology of

the majority of species in this clade. For example, numerous

basidiomycete yeasts can be isolated from soil and plant and

animal substrates and grown on synthetic media, but little is

known about how they function in nature (Fell et al. 2001).

Even within the mushroom-forming basidiomycetes, our

knowledge is limited usually to where they grow, if that, and

the details about what they do and how they manage to successfully

establish and compete often remain obscure.

Phylogeny

The traditional taxonomy of basidiomycetes was based largely

on the morphology of fruiting bodies and basidia. Since the

late 1980s, understanding of the phylogenetic relationships

of basidiomycetes has been revolutionized through the use

of molecular characters, especially sequences of ribosomal

genes (rDNA). Three major clades are recognized now:

Urediniomycetes, Ustilaginomycetes, and Hymenomycetes

(fig. 12.6; Swann and Taylor 1995). The branching order

among these three groups is not well resolved by rDNA data;

however, this is one area where additional data from genome

studies may help add resolution.

The Urediniomycetes consist of roughly 7400 (34%) of

the described species of basidiomycetes (Swann et al. 2001,

Hawksworth et al. 1995, Kirk et al. 2001). Members of

Urediniomycetes include yeasts and filamentous forms, which

function as saprotrophs and pathogens of plants, animals, and

fungi. When they occur, fruiting bodies in this group usually

are small and inconspicuous (Swann et al. 2001). Monophyly

of Urediniomycetes appears to be supported by biochemical

features of cell wall composition (cell wall sugars; Prillinger

et al. 1993), ultrastructural aspects of the hyphal septa, and

Figure 12.7. Basidiomycota life cycle. The haploid hyphal

individual mates early in the life cycle and then persists as a

dikaryon, so basidiomycetes found in nature are most often

dikaryons. Both haploid and dikaryotic individuals are able to

reproduce clonally via conidia in some species. Completion of

the sexual cycle involves nuclear fusion in basidia, followed

immediately by meiosis to produce basidiospores. Basidia and

basidiospores in some groups are produced on basidioma made

of dikaryotic hyphae, for example, mushrooms. Conidia and

basidiospores germinate to produce hyphae.

The Fungi 181

other characters that are visible only with transmission electron

microscopy (Swann et al. 1999, 2001).

The Urediniomycetes are divided into six major clades

(fig. 12.6). Relationships among the clades, however, are

poorly resolved by rDNA data. By far the largest clade in

Urediniomycetes is the Urediniomycetidae, which includes

more than 7000 species, most of which are the plant pathogenic

rusts (Uredinales). One intriguing member of Uredinomycetidae

is Septobasidium, which parasitizes colonies of living

scale insects as they feed on plant sap. Some groups now recognized

as Urediniomycetes were formally classified among

distantly related groups of fungi. For example, the Microbotryomycetidae

include anther smuts that were formerly

placed along with true smuts in Ustilaginomycetes (fig. 12.6).

Similarly, Mixia osmundae, a fern parasite, was once thought

to be a member of the ascomycetes, but rDNA data clearly place

it in the Urediniomycetes (Nishida et al. 1995). Recognition

of the monophyletic Urediniomycetes is a triumph of fungal

molecular systematics. Nevertheless, the lack of resolution

among the major clades remains a barrier to understanding

pathways of morphological and ecological evolution in this

group.

The Ustilaginomycetes contain about 1300 (6%) of the

described species of basidiomycetes (Bauer et al. 2001, Hawksworth

et al. 1995, Kirk et al. 2001) and includes plant parasites,

which often are dimorphic with a saprotrophic yeast

phase. Smuts of corn, barley, and wheat are economically important

members of this group. Corn smut (Ustilago maydis)

produces a large gall on maize ears that is eaten in the traditional

cuisine of Mexico, as cuitlacoche. Monophyly of Ustilaginomycetes

has received strong support in analyses of nSSU

rDNA sequences (Swann and Taylor 1993) but only moderate

support in more densely sampled studies of nuclear large subunit

rDNA sequences (Begerow et al. 1997). The composition

of cell wall sugars and ultrastructural aspects of host–fungus

interaction provide additional characters that support monophyly

of the Ustilaginomycetes (Bauer et al. 2001).

Three major clades have been recognized within Ustilaginomycetes:

Entorrhizomycetidae, Ustilaginomycetidae, and Exobasidiomycetidae

(fig. 12.6). The Exobasidiomycetidae are not

strongly supported as monophyletic by rDNA data, however,

and the branching order among the three clades is not well

resolved. Bauer et al. (2001) have developed a detailed classification

of Ustilaginomycetes (fig. 12.6) and have inferred

patterns of evolution of morphological characters and host

associations.

The Hymenomycetes include about 13,500 (60%) of the

described species of basidiomycetes (Swann and Taylor 1993,

Hawksworth et al. 1995, Kirk et al. 2001). A unifying character

for this group is the production of a “dolipore” septum

between cells. Typically, the dolipore septum is flanked by

a membrane bound structure termed a parenthesome, the

configuration of which is useful for delimiting major groups

within Hymenomycetes. Diverse fruiting bodies are formed

in Hymenomycetes, including some of the most complex

forms that have evolved within the fungi.

The Hymenomycetes consist of seven main clades; six of

them (Tremellales, Trichosporonales, Filobasidiales, Cystofilobasidales,

Dacrymycetales, and Auriculariales) include many

members of the heterobasidiomycetes sensu Wells and Bandoni

(2001), and the seventh (homobasidiomycetes) includes the

better known mushrooms, shelf fungi, and puffballs (fig. 12.6).

The heterobasidiomycetes encompass a tremendous range of

morphologies, including yeasts and filamentous forms, and a

wide range of ecological modes, including saprotrophs and

parasites of fungi and animals. Fruiting bodies of heterobasidiomycetes

are typically gelatinous and translucent, giving rise

to the common name “jelly fungi.” Familiar examples include

“witches butter” (Tremella mesenterica) and the edible woodear

(Auricularia auricula-judae), which is cultivated in Asia.

The homobasidiomycetes include more than 90% of the

species in Hymenomycetes, suggesting that this group has

undergone an increase in diversification rate relative to heterobasidiomycetes.

Homobasidiomycetes include the mushroomforming

fungi, which display an incredible diversity of fruiting

body forms. Yeast phases are generally absent from this group.

Traditionally, taxonomy of homobasidiomycetes depended on

morphological and anatomical characters of fruiting bodies.

This group has been sampled intensively by fungal systematists

(Bruns et al. 1998, Moncalvo et al. 2002, Hibbett et al.

2000). Although many aspects of morphology-based classifications

have been upheld, there have also been major rearrangements,

especially concerning the placement of the

taxonomically enigmatic gasteromycetes, such as puffballs,

false truffles, earthstars, and stinkhorns (Hibbett et al. 1997).

Hibbett and Thorn (2001) proposed a classification of the

homobasidiomycetes that includes eight major clades

(fig. 12.6). Relationships among the clades are generally not

well resolved, however, and recent analyses suggest that there

are also some additional minor clades of homobasidiomycetes

(Hibbett and Binder 2002).

Conclusions

Taxonomy of basidiomycetes has progressed dramatically in

recent years, but significant questions remain. Relationships

within and among major clades are often unresolved, which

limits understanding of the pathways of evolution in basidiomycetes,

and their role in the evolution of ecosystems. One

major class of questions concerns the causes of the different

patterns of apparent species richness observed from clade to

clade. For example, why are homobasidiomycetes and rusts

so diverse? The diversity seems too great simply to be due to

the ease with which large mushrooms are recognized or to

the intense economic interest in rusts. Did these two groups

diversify in response to some environmental change, such

as the rise of angiosperms, or are there intrinsic properties

of these groups that contributed to their success?

182 The Relationships of Fungi

Zygomycota

Species of the Zygomycota (Gr. zygos, marriage pairing;

mykes, fungi) are remarkable for their morphological and

ecological diversity (Hawksworth et al. 1995, Kirk et al.

2001), even though they account for fewer than 2% of all

described fungal species. This group includes fast-growing

molds responsible for storage rots of fruits, such as peaches

and strawberries. Other species can cause life-threatening

infections in humans and other animals, especially in immunocompromised

or artificially immunosuppressed patients

and diabetics (Rinaldi 1989). Most of the approximately 1000

described members of Zygomycota, however, are not encountered

by humans and lack common names because of their

microscopic size coupled with the fact that approximately

half of the species cannot be cultured axenically. Economically

and ecologically, the most important zygomycetes are

represented by Glomales, whose members are all asexual,

obligate symbionts of the great majority of vascular plants

(Sanders 1999, Redecker et al. 2000b, SchьЯler et al. 2001).

This specialized fungus–plant root symbiosis (mycorrhizae;

Gr. mykes, fungi; rhiza, root) functions as an auxiliary root

system that is critical for ecosystem function and plant diversity.

The mycorrhizal symbiosis is vital for phosphate

uptake by plants, especially in nutrient-poor soils. In addition,

such fungi are hypothesized to have been instrumental

in the colonization of land by the first terrestrial plants

(Pirozynski and Malloch 1975, Simon et al. 1993). Molecular

clock estimates indicate that Glomales diverged after the

divergences among zoosporic fungi (Chytridiomycota), at

least 600 Mya and possibly as much as 1.2–1.4 billion years

ago (Heckman et al. 2001, Berbee and Taylor 2001). Extant

glomalean species are remarkably similar to fossils from the

Ordovician period 460 Mya (Redecker et al. 2000a).

Beneficial species within Mucorales are used in the production

of the traditional east Asian soybean-based fermented

foods sufu (i.e., Chinese cheese) and tempeh. Another species

within the Murorales, Phycomyces blakesleeanus, is used

as a model system for understanding the genetics of phototropism

and sensory transduction, in part because it responds

to light over the same range as the human eye (Eslava and

Alvarez 1996). Species within the Entomophthorales (Gr.

entoma, insect; phthora, destroyer) have enormous potential

as natural biological control agents of pest insects.

Characteristics and Life Cycle

Although there are relatively few species of Zygomycota,

compared with Ascomycota and Basidiomycota, they exhibit

a remarkable diversity of life history strategies and ecological

specializations. Zygomycota species function as ecto- and

endomycorrhizal symbionts of vascular plants, obligate mycoparasites,

entomopathogens, endocommensials of aquatic

arthropods, terrestrial saprobes, and endo- or ectoparasites

of protozoa, nematodes, and other invertebrates (Benjamin

1979). A generalized life cycle is presented in figure 12.8.

Hyphal thalli typically consist of branched or unbranched

tubular filaments (fig. 12.9A) that either are predominately

nonseptate (i.e., coenocytic: Mucorales, Entomophthorales,

Glomales, and some Zoopagales and Endogonales) or are

regularly septate (Kickxellales, Dimargaritales, Harpellales,

and some Zoopagales). Where known, thalli have cell walls

composed of chitin plus chitosan or chitin plus b-glucan

(Bartnicki-Garcia 1987). Septa or cross walls are simple partitions

in hyphae, except in the Harpellales, Kickxellales, and

Dimargaritales, where they are flared with a plugged central

pore. Species-specific differences in the mating system determine

whether thalli are self-fertile (i.e., homothallic) or

self-sterile (i.e., heterothallic, requiring the union of thalli of

different mating types). Sexual reproduction, where known,

involves the fusion of differentiated (fig. 12.9B) or undifferentiated

hyphae followed by the development of a variously

enlarged unicellular zygosporangium (fig. 12.9C–E), within

which is formed a single zygospore. The zygospore is the only

diploid stage in the life cycle and the site of meiosis. Relatively

few studies have documented meiosis and zygospore

germination, in part because these thick-walled spores require

a dormancy period before they germinate to give rise

to a haploid mycelium. Although this group derives its name

from the sexual stage, phylogenetic studies are needed to

assess whether the zygospore is synapomorphic for this

group. Zygomycota also are united by the production of

asexual nonflagellated mitospores in uni- to multispored

sporangia (fig. 12.9F–O). Asexual spores also can be produced

as intercalary or terminal modifications of the vegetative

mycelium, or very rarely as a yeastlike phase. Mitospores

are passively released, except in Entomophthorales, where

they frequently are ejected forcibly (fig. 12.9k), and in the

coprophilic mucoralean genus Pilobolus (Gr. pileos, hat; bolus,

to throw), where the entire sporangium is discharged as far

as 2 m toward light.

Although members of the largest order, Mucorales,

comprise only one-third of all described Zygomycota taxa,

they represent the overwhelming majority of zygomycetous

species in axenic culture because they all grow saprobically

(O’Donnell 1979). Representatives of the other seven orders

account for less than half of all members of Zygomycota

in culture, in part because they include obligate parasites

(Dimigaritales, Zoopagales, and many Entomophthorales),

obligate arthropodphilous symbionts (Harpellales), and

ecto- and endomycorrhizal species (Endogonales and

Glomales, respectively). Except for one mycoparasitic species,

all Kickxellales species can be cultivated axenically.

Mycoparasitic species of Dimargaritales and Zoopagales

typically are cultured on their mucoralean hosts, but some

of these species can be grown axenically on specialized

media (Benjamin 1979). Specific culture collections have

been established for Entomophthorales (Humber and

Hansen 2003) and Harpellales (Lichtwardt et al. 2001). In

addition, several phylogenetically diverse collections of the

The Fungi 183

on morphological apomorphies, nutritional mode, and ecological

specialization, are monophyletic except for Mortierellaceae,

which may not form a monophyletic group with the

Mucorales (Gehrig et al. 1996). Three orders of Zygomycota

described recently (Cavalier-Smith 1998) are not accepted

here, however, because Geosiphonales appears to be nested

within Glomales, and too few data are available to assess the

phylogenetic validity Mortierellales and Basidiobolales. Also,

a new group, Glomeromycota, proposed to accommodate

Glomales sensu Schwarzott et al. (2001), is based primarily

on SSU rRNA data. It should be considered provisional until

more robust molecular phylogenetic data become available.

Recent molecular phylogenies have advanced our knowledge

of Zygomycota by providing novel hypotheses of evolutionary

relationships within Glomales (Simon et al. 1993,

Gehrig et al. 1996, Redecker et al. 2000b, SchьЯler et al.

2001, Schwarzott et al. 2001), Harpellales and Kickxellales

(Gottlieb and Lichtwardt 2001, O’Donnell et al. 1998), Entomophthorales

(Jensen et al. 1998), Mucorales (O’Donnell

et al. 2001), and Dimargaritales and Zoopagales (Tanabe et al.

2000). Two classes have been recognized in all recent taxonomic

schemes for Zygomycota (Benny 2001, Benny et al.

2001): Trichomycetes (Gr. thrix, hair; mykos, fungi), represented

by four arthropodophilous orders, Amoebidiales,

Harpellales, Eccrinales and Ascellariales (Lichtwardt 1986);

and Zygomycetes. However, polyphyletic Trichomycetes is

not accepted here. Molecular phylogenetic analyses based on

SSU rRNA indicate members of Amoebidiales are protists

(Ustinova et al. 2000, Benny and O’Donnell 2000), as long

suspected because their cell walls lack chitin and they produce

amoeboid cells, which otherwise are unknown in Fungi

(although some zoospores of Chytridiomycota can exhibit

amoeboid movement). Phylogenetic evidence from SSU

rRNA data also has identified Harpellales as a sister group

to a Spiromyces + Kickxellales clade or to Spiromyces within

Zygomycetes (Gottlieb and Lichtwardt 2001, James et al.

2000, O’Donnell et al. 1998). Lastly, Eccrinales and Asellariales

are treated as incertae sedis until their phylogenetic

relationships are resolved.

Chytridiomycota

Chytridiomycota are a relatively poorly known group at the

base of the fungal tree, accounting for 1% or 2% of described

fungal species. Chytridiomycetes, or chytrids, as they commonly

are known, are microscopic and have a simple morphology.

The distinguishing feature of the group is reproduction

through a motile zoospore. The chytridiomycete zoospore

typically possesses a single, smooth flagellum that is inserted

on the cell posterior to the direction of motility. The chytridiomycetes

have been variously classified through the years with

other fungi and protists; as recently as 1990 Chytridiomycota

were placed in Protoctista (Barr 1990). Because they produce

zoospores, chytrids are generally thought to be aquatic fungi.

Figure 12.8. Generalized Zygomycota life cycle. Individuals in

nature typically are hyphal and haploid. Vegetative hyphae can

differentiate into reproductive structures for clonal (sporangia,

sporangiospores) or sexual reproduction (gametangia). Sexual

reproduction involves mating by gametangial fusion to produce

a diploid zygote. In almost all cases, there is no fruiting body

surrounding the zygospores. Both mature zygospores and

conidia germinate to produce haploid hyphae. In the case of

zygospores, the germinating hypha immediately differentiates to

make a sporangium and sporangiospores.

obligately mycorrhizal Glomales are available (http://invam.

caf.wvu.edu, http://res2.agr.ca/ecorc/ginco-can/ and http://

www.ukc.ac.uk/bio/beg/). In these collections, Glomales

species are maintained in vivo in host plants, stored as dried

inoculum, or kept as cryogenically preserved material, or

accessioned by all three methods.

Phylogenetic Relationships and Taxonomic Implications

Zygomycota appear to be non-monophyletic in most SSU

rRNA and some b-tubulin gene analyses. However, the

monophyly of this group has not been tested fully through

analyses of the available molecular phylogenetic data. These

analyses are based primarily on SSU rRNA (Bruns et al. 1992,

Gehrig et al. 1996, James et al. 2000, Jensen et al. 1998,

Nagahama et al. 1995, SchьЯler et al. 2001, Tanabe et al.

2000), b-tubulin (Keeling et al. 2000) and several proteincoding

genes within the mitochondrial genome (Forget et al.

2002, Lang 2001). Interestingly, Zygomycota may be monophyletic,

if the putative long-branch taxon Basidiobolus ranarum

(Entomophthorales), which clusters with Chytridiomycota in

unconstrained SSU rRNA analyses, is excluded from the analysis

[see James et al. (2000) for more information on Basidiobolus;

see the section on Chytridiomycota below).

Relationships among orders of Zygomycota are poorly

resolved by SSU rRNA phylogenies, except for a Harpellales

+ Kickxellales + Spiromyces clade (Gottlieb and Lichtwardt

2001, O’Donnell et al. 1998), with Zoopagales as a putative

sister group (Tanabe et al. 2000). Overall, the available SSU

data suggest that the orders as presently circumscribed, based

184 The Relationships of Fungi

This characterization is inaccurate, because they readily are

isolated from soil. Originally described in the 19th century

as curious “asterospheres” in living algae, these fungi have a

strong habitat association as parasites and saprophytes on

algae (Sparrow 1960). Chytrids, however, also play an important

role in the decomposition of recalcitrant substrates,

such as chitin, keratin, pollen, insect exuviae, plant debris,

and so forth (Powell 1993). As a group, chytrids are ubiquitous

in lakes, ponds, and soil. Many can be cultured, and the

current study of chytrids generally involves observations of

species in pure culture, whereas past descriptions focused

on “gross culture” or their study on freshly collected substrates.

Chytrids easily can be isolated from environmental

samples by baiting with appropriate substrates, for example,

pollen, cellophane, purified shrimp exoskeletons, and snake

skin (Barr 1987).

The chytridiomycetes may be regarded as the economically

least important major group of fungi, but there are several

notable exceptions. Neocallimastigales are a clade of

chytrids whose members are found in the rumen and hindgut

of mammalian herbivores, where they aid in the digestion

of plant fibers (Orpin 1988). Other economically important

chytrids are the generalist plant pathogens Synchytrium and

Physoderma. Species in both genera cause agricultural diseases

in tropical climes, and Synchytrium endobioticum causes plant

disease in the temperate zone. This parasite causes a malformation

of potato tubers known as black wart. As recently as

2000, it was responsible for a one-year total quarantine on

the importation of potatoes from Prince Edward Island into

the United States, resulting in a loss of at least $30 million

to Canadian farmers. Finally, chytrids are parasites also on

metazoans, primarily on soil invertebrates, such as nematodes

and tardigrades. A notable exception is the vertebrate pathogen

Batrachochytrium dendrobatidis, which infects frogs and

has been associated with the recent global trend of amphibian

declines (Berger et al. 1998, Longcore et al. 1999). If

Basidiobolus ranarum truly is a chytrid (see below), then this

amphibian and sometimes human pathogen would join

B. dendrobatidis as a chytrid pathogen of vertebrates.

Taxonomy

Chytridiomycota consist of five orders, containing approximately

120 genera and 1000 species (Longcore 1996). Blastocladiales

include Allomyces macrogynus, well known for studies

on its cytology, genetics, and physiology, and Coelomomyces

stegomyiae, a parasite of mosquito larvae. Fungi in this clade

are distinguished by zoospores with a prominent “nuclear cap”

of ribosomes. Monoblepharidales embrace only five genera;

these aquatic chytrids are rarely seen but can be collected on

decaying plant material such as fruits and twigs. Monoblepharids

are distinguished by oogamous sexual reproduction

(i.e., the female gamete is not motile and is larger than the

uniflagellate male gamete) and vacuolate cells. Members of

Spizellomycetales are ubiquitous in soil; one distinguishing

feature is the amoeboid movement of zoospores during swim-

Figure 12.9. Scanning electron micrographs of Zygomycota. (A) Coenocytic mycelium with

aerial hyphae beginning to form. (B–E) Sexual reproduction. (B) Gametangial fusion. (C–E)

Zygosporangia. (F–O) Asexual reproduction. (F) Aerial, terminal multispored sporangium with

basal rhizoids. (G) Multispored sporangium. (H and I) Few-spored sporangia. (J–L) Unispored

sporangia. (M) Vesiculate mycoparasite growing on mucoraceous host. (N) Terminal fertile vesicle

of mycoparasite. (O) Terminal fertile branch of a mycoparasite with two-spored sporangia.

d e

f h i j

k

g

l

m n o

a b c

The Fungi 185

ming (Barr 2001). Neocallimastigales are reserved for chytrids

that inhabit anaerobic, rumen, and hindgut environments.

These fungi either are uniflagellate or possess multiple flagella.

The final and largest order, Chytridiales (~80 genera), contains

a diversity of morphological forms. Most of the algal parasites

are found in this clade.

Morphology

Chytridiomycete classification, traditionally, has been based

on characteristics of vegetative growth and reproductive

structures. The primary reproductive structure is the sporangium,

a saclike structure whose contents are cleaved internally

into zoospores (fig. 12.10A,B). Sporangia generally

are subtended by a system of rhizoids that penetrate the

substrate and facilitate anchoring and nutrient absorption.

In some chytrids, the rhizoid system develops into an indeterminate,

interconnected group of filaments, termed a

rhizomycelium. Numerous sporangia can be produced from

a rhizomycelium, which typically is coenocytic and lacks true

septa. At maturity, zoospores are released from sporangia

either through a small rounded opening (papillus) or a discharge

tube. In some chytrids, the presence of a lidlike cover

at the site of zoospore release can be seen clearly. This structure,

the operculum, played an important role in previous

classifications of chytrids (fig. 12.10B; Sparrow 1960, Karling

1977). A final, distinguishing character of many chytrids is

the production of a resting spore. These thick-walled spores

are desiccation resistant and can germinate into a sporangium

after many years of dormancy. Although sexual reproduction

generally results in the production of a resting spore,

these spores also are produced asexually.

Life Cycle

Sexual reproduction has been observed in very few chytrids,

but the variety of described mating systems is excitingly varied.

Different modes of reproduction include the fusion of

zoospores, gametangia, or rhizoids with subsequent transformation

of the zygote into a resting spore (wherein meiosis is

believed to occur; Doggett and Porter 1996). Oogamous reproduction

occurs in Monoblepharidales, as mentioned above.

In some species of Blastocladiales, an alternation of generations

occurs between diploid sporophytes and haploid gametophytes.

Allomyces species are hermaphoditic in that both male

and female gametangia are produced on the same thallus.

Sexual reproduction has been observed neither in Spizellomycetales

nor in Neocallimastigales (Barr 2001). A representative

Chytridiales life cycle is shown in figure 12.11.

Ultrastructure

Most chytrids have a simple and variable body plan that presents

few characters on which to base a phylogentically

meaningful taxonomy. Consequently, their ultrastructure

as revealed by the transmission electron microscope is important

in classification. Useful characters have been discovered

in the zoospore (Lange and Olsen 1979); this

special spore has proven to be exceptionally informative

because of its internal complexity and conserved features

(fig. 12.12). The zoospore is bounded by a membrane but

lacks a cell wall. The zoospore of most chytrids contains a

nucleus associated with an electron dense microbody and

one to several lipid globules (fig. 12.12). The arrangement

of these organelles is called the microbody–lipid globule

complex and was used to group chytridiomycete zoospores

Figure 12.10. (A) Light micrograph of a developing sporangium

with rhizoids of Chytriomyces hyalinus. (B) Light micrographs of

zoospore discharge in Chytriomyces hyalinus showing an

operculum (O) and a lenticular, expanding net of fibers (L) that

constrains the zoospores for a brief period before they mature

and swim away. From Taylor and Fuller (1981).

Figure 12.11. Generalized Chytridiomycota life cycle. The

haploid thallus can differentiate to produce a zoosporangium

with clonal zoospores, or to mate and produce a resistant

sporangium. The resistant sporangium may germinate to release

zoospores. Upon finding a suitable substrate, zoospores form

cysts and the cysts germinate to produce a new thallus.

b

a

186 The Relationships of Fungi

into broad taxonomic categories (Powell 1978). Another

important feature of the zoospore is the rumposome, a fenestrated

membrane located near the posterior portion of

the zoospore adjacent to the spore membrane (Fuller and

Reichle 1968). This organelle has been observed only in

members of Chytridiales and Monoblepharidales. More recently,

emphasis has been placed on the fine details of the

flagellar apparatus (Barr 1990, 2001, James et al. 2000).

Important characters include the connection of the nonflagellated

centriole to the kinetosome (base of the flagellum)

and the arrangement of microtubules and other

kinetosomal roots. Zoospore ultrastructure currently is the

only phenotypic means of accurately classifying chytrids

into orders and even genera (Barr 1980, 2001).

Phylogenetic Relationships

Although the chytridiomycetes were recently classified in the

Protoctista (Barr 1990), the link between Chytridiomycota and

other members of Fungi already had been suggested by the

presence of chitinous cell walls, use of glycogen as a storage

molecule, and presence of flattened mitochondrial cristae

(Cavalier-Smith 1987, Powell 1993). Early phylogenies based

on nSSU rDNA confirmed that Chytridiomycota are part of a

monophyletic Fungi and are basal within Fungi (Fцrster et al.

1990, Dore and Stahl 1991, Bowman et al. 1992). The basal

position of Chytridiomycota in Fungi suggests that the common

ancestor of all fungi possessed motile zoospores. Therefore,

the retention of a zoospore stage by the chytrids is

considered a pleisiomorphy (ancestral character), which makes

tenuous the unification and classification of chytrids based on

the presence of a zoospore, because multiple independent

losses of the flagellum may have occurred. For this reason, it

is possible that Chytridiomycota is not a monophyletic group.

At present, few molecular phylogenetic data are available

for the chytrids. Relationships of Chytridiomycota to

other fungi have been examined, using primarily the SSU

rRNA gene (Li and Heath 1992, Bruns et al. 1992, Nagahama

et al. 1995, Jensen et al. 1998, James et al. 2000,

Tanabe et al. 2000). These data are unclear as to whether

the chytrids are monophyletic, because Blastocladiales typically

groups with Zygomycota, rendering Chytridiomycota

paraphyletic. In addition, placement of the putative zygomycete

Basidiobolus ranarum within Chytridiomycota in SSU

rRNA phylogenies has raised the possibility that some

zygomycete orders may be chytrids that have experienced

independent losses of the flagellum (Nagahama et al. 1995,

Jensen et al. 1998). In support of the multiple independent

losses of flagella is the observation that Basidiobolus species,

which lack flagella, harbor an organelle resembling the centriole-

like kinetosome found at the cellular end of flagella

in Chytridioimycota; no such organelle is found in Zygomycota

(McKerracher and Heath 1985). Confusing the picture

is the placement of B. ranarum in Chytridiales by nSSU

rDNA analyses but in Zygomycota by using b-tubulin analyses

(Keeling et al. 2000). One possible explanation is that

tubulin molecules evolve in similar ways when the constraint

of flagellar function is lost, as might have occurred

in B. ranarum and Zygomycota. The resolution of the possible

non-monoplyly of Chytridiomycota awaits further

sampling of genes and taxa.

Only one molecular phylogenetic study has heavily

sampled taxa within Chytridiomycota (James et al. 2000).

The authors of this study concluded that zoospore ultrastructure

was concordant with the SSU rRNA phylogeny

and that the five orders of chytrids seem to be monophyletic,

with the exception of the largest order, Chytridiales.

Within Chytridiales, well-supported clades were found, and

these were consistent with groupings based on zoospore

ultrastructure. However, relationships among clades of

Chytridiales as well as among the orders were unresolved.

Molecular phylogenies also confirmed the suspicion that

chytrid gross morphology is of little use in classification.

Indeed, pure culture studies have shown plasticity of devel-

Figure 12.12. Ultrastructure of a typical Chytridiales zoospore

as exemplified by Podochytrium dentatum. G, Golgi apparatus;

K, functional kinetosome at the base of the flagellum; L, lipid

globule; M, mitochondrion; mb, microbody; mt, microtubules;

N, nucleus; nfc, second (nonfunctional) kinetosome;

O, transition-zone plug; P, prop; pl, plates; R, ribosomes;

Ru, rumposome; SI, striated inclusion; Va, vacuole. From

Longcore (1992).

The Fungi 187

opmental characters previously thought to be important in

chytrid classification (Roane and Paterson 1974, Powell and

Koch 1977). In contrast, zoospore ultrastructure has proven

to be quite informative, and further investigation of these

characters is warranted.

Studies of other gene regions also have shed some light

on phylogenetic relationships of the chytridiomycetes. As

mentioned above, analyses of b-tubulin gene sequences conflict

with nSSU rDNA analyses over the placement of

Basidiobolus (Keeling et al. 2000). Unfortunately, b-tubulin

sequences show minimal variation among chytrids and provide

little resolution of relationships among orders, making

it imperative to examine other protein-coding genes to understand

relationships of Chytridiomycota and Zygomycota.

One promising development is the effort of the Fungal Mitochondrial

Genome Project, which has sequenced the entire

mitochondrial genome of several chytrids (Paquin et al. 1997,

Forget et al. 2002, Bullerwell et al. 2003). Their analyses with

concatenated mitochondrial proteins suggest a Spizellomycetales

+ Chytridiales clade, with Monoblepharidales as a

sister group. These data also show a paraphyletic Chytridiomycota

because Allomyces (Blastocladiales) again groups

with the nonzoosporic fungi (including Zygomycota). Unfortunately,

analysis of whole mitochondrial genomes must

exclude the amitochondriate Neocallimastigales. In analyses

of SSU rRNA, however, these fungi appear to be allied to

Spizellomycetes, the order in which they previously were

placed (Heath et al. 1983).

Based on current knowledge, it is possible to suggest a

plausible phylogenetic hypothesis for Chytridiomycota for

future testing (fig. 12.13). We may have been conservative

in treating Chytridiomycota and Zygomycota as monophyletic

groups and not as non-monophyletic groups, as shown

in figures 12.2 and 12.13. However, until data from additional

genes and taxa are available, we prefer to consider the

treatment in figure 12.13 to be a hypothesis. In addition,

more diversity continues to be uncovered as new chytrids

are described and investigated with the electron microscope

(Nyvall et al. 1999). Characterizing this diversity at the molecular

level may result in the discovery of new major clades.

Fungi and Geologic Time

Our knowledge of the geologic history of Fungi is the subject

of debate, mostly because of a lack of good fossils. The

fossil record for fungi is based on very few specimens compared

with that for plants and animals, probably because of

a combination of factors: (1) fungi are mostly microscopic

and are therefore easy to miss, (2) their tissues do not preserve

very well, and (3) there are relatively few paleontologists

looking for fungal fossils. Indeed, many of the best fossils

are known only in association with a preserved plant or animal

host. Some very well preserved fossils have been discovered,

but they provide only a few, hazy pictures of the long

history of fungi. The oldest convincing fossils of Fungi were

discovered in the Ordovician (~460 Mya) of Wisconsin, as

hyphae and spores that strongly resemble modern structures

in the genus Glomus (Redecker et al. 2000a). Otherwise, the

vast majority of the oldest fungal fossils come from a single

site, the lower Devonian (~400 Mya) Rhynie Chert of Scotland.

A wide variety of fossils have been taken from this location,

mostly members of Zygomycota and Chytridiomycota

(Taylor and Taylor 1997). These fossils include zygomycete

lichens associated with probable cyanobacterial photobionts

(Taylor et al. 1995a, 1997), chytrid fungi resembling members

of the modern genera Allomyces (Blastocladiales; Taylor

et al. 1994, Remy et al. 1994a) and Entophlyctis (Chytridiales;

Taylor et al. 1992), and glomalean fungi (Remy et al. 1994b,

Taylor et al. 1995b). Most surprising, fossils morphologically

very similar to extant members of Sordariomycetes (Ascomycota)

were identified in the Rhynie Chert associated with

the early land plant Asteroxylon (Taylor et al. 1999). The Rhynie

Chert fossils indicate that a wide variety of fungi were present

in the early Devonian period, including some resembling

modern taxa thought to have evolved much more recently.

With few fossils available, analysis of DNA sequence is

an attractive and powerful tool for inferring the times of origin

for the major groups of Fungi. Different sets of molecular

data have been used for these analyses and different

analyses have used different calibration times for the divergence

of animals and fungi; their results are summarized in

table 12.1. Most approaches to date divergence times of organisms

assume a molecular clock, where a rate of sequence

evolution is identified for a particular gene region, and use a

known calibration point, for example, the age of a known

Figure 12.13. Phylogenetic relationships of Chytridiomycota

orders to other fungi.

188 The Relationships of Fungi

fossil or an independently estimated divergence time for fungi

and animals. With these assumptions and data, divergence

times between fungal divergences can be estimated. The first

comprehensive attempts to date fungal divergences used

nSSU rDNA and dated the origin of terrestrial fungi from the

aquatic chytrids at approximately 550 Mya, in the Cambrian

(Berbee and Taylor 1993). Using the knowledge that Fungi

and Animalia probably share a common ancestor (Wainright

et al. 1993), and a date of 965 Mya for that divergence

(Doolittle et al. 1996), Berbee and Taylor (2001) revised their

estimates based on nSSU rDNA and found that most inferred

divergence times were pushed 50–100 million years earlier.

Using the revision of Feng et al. (1997) for the divergence of

animals and fungi, from 965 to 1200 Mya, would only have

increased that effect. Berbee and Taylor (2001) used one gene

for which sequences from many taxa were available, but more

recent studies have used the ever-expanding DNA sequence

databases to analyze more genes from fewer taxa. Wang et al.

(1999) used amino acid sequences from 50 genes to explore

the origin of animals, plants, and fungi. Although the majority

of genes supported animals and fungi as closest ancestors,

others supported animal and plant or plants and fungi

as closest relatives, with an estimate of approximately 1576

Mya for the origin of these three kingdom-like clades. Using

this and other molecular calibration points, Heckman et al.

(2001) used amino acid sequences from 119 genes to estimate

the divergence times of the major groups of fungi and

inferred that most major groups evolved deep in the Precambrian,

long before the points from which we have good fossils.

These authors note that nSSU rDNA data give a similar

result, provided that a date of about 1576 Mya is used for

the divergence of animals and fungi. This result leaves us to

wonder what fungi were doing on Earth for a billion years

before they were preserved as the fossils we know to exist. A

point strongly in favor of the older estimate for the divergence

of animals and fungi is the multiple gene estimate of

~670 Mya for the divergence of Sordariomycetes, which accommodates

the discovery of a 400 Mya sordariomycete fossil

from the lower Devonian. The age of this fossil is in conflict

with the SSU estimate of ~310 Mya for the sordariomycete

divergence, which is calibrated by a divergence of animals

and fungi of 900 Mya (table 12.1).

In summary, both newly discovered fossils and molecular

data have pushed back our estimates of the origins of the

major fungal groups (Taylor et al. 1999, Redecker et al.

2000a, Berbee and Taylor 2001, Heckman et al. 2001). Ancient

origins of fungi strongly suggest that fungi played an

important role in the early colonization of land by plants and

animals, both by changing the physical and chemical environment

and by establishing mutualistic symbioses such as

mycorrhizae and lichens (Selosse and Le Tecon 1998,

Redecker et al. 2000b, Lutzoni et al. 2001, Heckman et al.

2001). The discrepancies between the history of fungi told

by the fossil record and that by a molecular clock suggest that

far more data are needed. Precambrian sources should be

analyzed further for fungal fossils, and reports of Silurian

fossils of Ascomycota (Sherwood-Pike and Gray 1985) deserve

renewed attention. New methods of analysis that can

Table 12.1

Divergence Times within Major Fungal Groups.

Age of oldest

rDNAa rDNAb 119 protein known fossil

estimate estimate genec estimate in ref. group

Groups compared (reference group in parentheses) (Mya) (Mya) (Mya) (Mya)

(Chytridiomycota) versus Zygomycota + Ascomycota + Basidiomycota ~550 ~660 1458 ± 70 ~400d

Chytridiomycota + (Zygomycota) versus Ascomycota + Basidiomycota ~490 ~590 1107 ± 56e ~460f

(Ascomycota) versus Basidiomycota ~390 ~560 1208 ± 108 ~400g

(Hymenomycetes) versus Ustilaginomycetes ~380 ~430 966 ± 86 ~290h

(Taphrinomycotina) versus Saccharomycotina + Pezizomycotina ~320 ~420 1144 ± 77 None

Saccharomycotina versus (Pezizomycotina) ~310 ~370 1085 ± 81 ~400g

Eurotiomycetes versus (Sordariomycetes) ~290 ~310 670 ± 71 ~400g

aMolecular clock calibrated using fungal fossils (Berbee and Taylor 1993).

bMolecular clock calibrated using fungal fossils and divergence time of fungi vs. animals estimated at 965 Ma (Doolittle et al. 1996, Berbee and

Taylor 2001).

cMolecular clocks calibrated using divergence of plants, animals, and fungi estimated at 1576 Mya, divergence of nematodes and arthropods at

1177 Mya, and arthropods and chordates at 993 Mya, each of which was in turn based on a 75-gene molecular clock calibrated with the vertebrate

fossil record (Heckman et al. 2001).

dSeveral different fossilized chytrids from Rhynie Chert (Taylor and Taylor 1997).

eNo glomalean fungi were included in this study. The Glomales, which represent the oldest reliable fungi in the fossil record, are probably the

most recently derived major clade of the Zygomycota.

fFossilized glomalean spores and hyphae from the Ordovician period (Redecker et al. 2000a).

gFossilized Pyrenomycete from Rhynie Chert (Taylor et al. 1999).

hFossilized hyphae with clamp connections (Dennis 1970).

The Fungi 189

accommodate rate variation among lineages (e.g., Sanderson

2002) should be investigated and compared with other methods.

Our current estimates of the timing of events in fungal

evolution undoubtedly are crude and are sure to be improved

as data and methods improve. However, it is essential that

they be made, even knowing that they can be improved,

because time is the common currency of evolutionary biologists,

and only by making such estimates can events in the

history of Fungi be compared with those in the other major

kingdom-like groups. We hope that those who design museum

displays will note these efforts and include fungi in their

work.

Last Word

Looking back on a dozen years of fungal molecular phylogenetics,

it is clear that no approach since microscopy has

had such a profound influence on our understanding of fungal

evolution. Owing to their microscopic size and ability to

live in their food, fungi are cryptic in a way that no angiosperm

or vertebrate can imitate. This fact has made the research

of fungal molecular phylogenetics even more valuable,

because it enables ecologists, finally, to add the fungi to their

studies. Over the next decade, we look forward to the improved

phylogenetic resolution that genomics and improved

analytical methods promise, and to the application of microarray

technology to ecological studies. The latter should automate

fungal identification and make it possible to more

accurately estimate fungal biodiversity. That information

should provide some further surprises and it seems sure to

close the gap between the 100,000 described fungi and the

1.5 million estimated to exist in nature.

Acknowledgments

We thank Joyce Longcore for advice on the manuscript and

Zheng Wang for the illustrations used in figure 12.6. We

acknowledge the support of the National Science Foundation

(Research Coordination Networks in Biological Sciences: A

Phylogeny for Kingdom Fungi; NSF 0090301).

Literature Cited

Agrios, G. N. 1997. Plant pathology. 4th ed. Academic Press,

San Diego.

Alexopoulos, C. J., C. W. Mims, and M. Blackwell. 1996.

Introductory mycology. John Wiley and Sons, New York.

Arnold, A. E., Z. Maynard, and G. S. Gilbert. 2001. Fungal

endophytes in dicotyledonous neotropical trees: patterns of

abundance and diversity. Mycol. Res. 105:1502–1507.

Barnett, J. A., R. W. Payne, and D. Yarrow. 1990. Yeasts:

characteristics and identification. Cambridge University

Press, Cambridge.

Barr, D. J. S. 1980. An outline for the reclassification of the

Chytridiales, and for a new order, the Spizellomycetales.

Can. J. Bot. 58:2380–2394.

Barr, D. J. S. 1987. Isolation, culture and identification of

Chytridiales, Spizellomycetales, and Hyphochytriales.

Pp. 118–120 in Zoosporic fungi in teaching and research

(M. S. Fuller and A. Jaworski, eds.). Southeastern Publishing,

Athens, GA.

Barr, D. J. S. 1990. Phylum Chytridiomycota. Pp. 454–466

in Handbook of Protoctista (L. Margulis, J. O. Corliss,

M. Melkonian, and D. J. Chapman, eds.). Jones and Bartlett,

Boston.

Barr, D. J. S. 2001. Chytridiomycota. Pp. 93–112 in The mycota

VIIA, systematics and evolution (D. J. McLaughlin, E. G.

McLaughlin, and P. A. Lemke, eds.). Springer-Verlag, Berlin.

Barron, G. L. 1988. Microcolonies of bacteria as a nutrient

source for lignicolous and other fungi. Can. J. Bot.

66:2505–2510.

Bartnicki-Garcia, S. 1987. The cell wall: a crucial structure in

fungal evolution. Pp. 389–403 in Evolutionary biology of

the fungi (A. D. M. Rayner, C. M. Brasier, and D. Moore,

eds.). Cambridge University Press, Cambridge.

Bauer, R., D. Begerow, F. Oberwinkler, M. Piepenbring, and

M. L. Berbee. 2001. Ustilaginomycetes. Pp. 57–84 in The

mycota VIIB, systematics and evolution (D. J. McLaughlin,

E. G. McLaughlin, and P. A. Lemke, eds.). Springer-Verlag,

Berlin.

Begerow, D., R. Bauer, and F. Oberwinkler. 1997. Phylogenetic

studies on nuclear large subunit ribosomal DNA sequences

of smut fungi and related taxa. Can. J. Bot. 75:2045–2056.

Benjamin, R. K. 1979. Zygomycetes and their spores. Pp.573–

616 in The whole fungus. The sexual-asexual synthesis

(B. Kendrick, ed.), vol. 2. Museums of Canada and the

Kananaskis Foundation, Ottawa.

Benjamin, R. K., M. Blackwell, I. Chapella, R. A. Humber, K. G.

Jones, K. A. Klepzig, R. W. Lichtwardt, D. Malloch,

H. Noda, R. A. Roeper, J. W. Spatafora, and A. Weir. In

press. The search for diversity of insects and other arthropod

associated fungi. In Biodiversity of fungi: standard

methods for inventory and monitoring (G. M. Mueller, G. F.

Bills, and M. Foster, eds.). Academic Press, New York.

Benny, G. L. 2001. Zygomycota: Trichomycetes. Pp. 147–160

in The mycota VIIA, systematics and evolution (D. J.

McLaughlin, E. G. McLaughlin, and P. A. Lemke, eds.).

Springer-Verlag, Berlin.

Benny, G. L., R. A. Humber, and J. B. Morton. 2001.

Zygomycota: Zygomycetes. Pp. 113–146 in The mycota

VIIA, systematics and evolution (D. J. McLaughlin, E. G.

McLaughlin, and P. A. Lemke, eds.). Springer-Verlag, Berlin.

Benny, G. L., and K. O’Donnell. 2000. Amoebidium parasiticum

is a protozoan, not a Trichomycete. Mycologia 92:1133–

1137.

Berbee, M. L. 1998. Loculoascomycete origins and evolution of

filamentous ascomycete morphology based on 18S rRNA

gene sequence data. Mol. Biol. Evol. 13:462–470.

Berbee, M. L., and J. W. Taylor. 1992. Convergence in ascospore

discharge mechanism among Pyrenomycete fungi

based on 18S ribosomal RNA gene sequence. Mol.

Phylogenet. Evol. 1:59–71.

Berbee, M. L., and J. W. Taylor. 1993. Dating the evolutionary

radiations of the true fungi. Can. J. Bot. 71:1114–1127.

190 The Relationships of Fungi

Berbee, M. L., and J. W. Taylor. 2001. Fungal molecular

evolution: gene trees and geologic time. Pp. 229–245 in The

mycota VIIB, systematics and evolution (D. J. McLaughlin,

E. G. McLaughlin, and P. A. Lemke, eds.). Springer-Verlag,

Berlin.

Berger, L., R. Speare, P. Daszak, D. E. Green, A. A.

Cunningham, C. L. Goggin, R. Slocombe, M. A. Ragan,

A. D. Hyatt, K. R. McDonald, et al. 1998. Chytridiomycosis

causes amphibian mortality associated with population

declines in the rain forests of Australia and Central America.

Proc. Natl. Acad. Sci. USA 95:9031–9036.

Bhattacharya, D., F. Lutzoni, V. Reeb, D. Simon, and

F. Fernandez. 2000. Widespread occurrence of spliceosomal

introns in the rDNA genes of Ascomycetes. Mol. Biol.

Evol. 17:1971–1984.

Blackwell, M. 2000. Perspective: Evolution: Terrestrial life—

fungal from the start? Science 289:1884–1885.

Bowman, B. H., J. W. Taylor, J. L. Brownlee, S.-D. Lu, and T. J.

White. 1992. Molecular evolution of the fungi: relationship

of the Basidiomycetes, Ascomycetes, and Chytridiomycetes.

Mol. Biol. Evol. 9:258–296.

Brodo, I. M., S. Duran Sharnoff, and S. Sharnoff. 2001. Lichens

of North America. Yale University Press, New Haven, CT.

Bruns, T. D., T. M. Szaro, M. Gardes, K. W. Cullings, J. Pan,

D. L. Taylor, and Y. Li. 1998. A sequence database for the

identification of ectomycorrhizal fungi by sequence analysis.

Mol. Ecol. 7:257–272.

Bruns, T. D., R. Vilgalys, S. M. Barns, D. Gonzalez, D. S.

Hibbett, D. J. Lane, L. Simon, S. Stickel, T. M. Szaro, W. G.

Weisburg, and M. L. Sogin. 1992. Evolutionary relationships

within the Fungi: analyses of nuclear small subunit

rRNA sequences. Mol. Phylogenet. Evol. 1:231–241.

Bullerwell, C. E., L. Forget, and B. F. Lang. 2003. Evolution of

monoblepharidalean fungi based on complete mitochondrial

genome sequences. Nucleic Acids Res. 31:1614–1623.

Carroll, G. 1988. Fungal endophytes in stems and leaves: from

latent pathogen to mutualistic symbiont. Ecology 69:2–9.

Carroll, G. 1995. Forest endophytes: pattern and process. Can.

J. Bot. 73:S1316–S1324.

Carroll, G. C., and D. T. Wicklow, 1992. The fungal community:

its organization and role in the ecosystem. Marcel

Dekker, New York.

Cavalier-Smith, T. 1987. The origin of Fungi and pseudofungi.

Pp. 339–353 in Evolutionary biology of the fungi (A. D. M.

Rayner, C. M. Brasier, and D. Moore, eds.). Cambridge

University Press, Cambridge.

Cavalier-Smith, T. 1998. A revised six-kingdom of life. Biol.

Rev. 73:203–266.

Chapela, I., S. A. Rehner, T. R. Schultz, and U. G. Mueller.

1994. Evolutionary history of the symbiosis between

fungus-gorwing ants and their fungi. Science 266:1691–

1694.

Clay, K. 2001. Symbiosis and the regulation of communities.

Am. Zool. 41:810–824.

Cole, G. T., and B. Kendrick. 1981. Biology of conidial fungi.

Academic Press, New York.

Cullen, D. 1997. Recent advances on the molecular genetics of

ligninolytic fungi. J. Biotechnol. 53:273–289.

Currie, C. R., B. Wong, A. E. Stuart, T. R. Schultz, S. A. Rehner,

U. G. Mueller, G. H. Sung, J. W. Spatafora, and N. A.

Straus. 2003. Ancient tripartite coevolution in the attine

ant-microbe symbiosis. Science 299:386–388.

Dennis, R. L. 1970. A Middle Pennsylvanian basidiomycete

mycelium with clamp connections. Mycologia 62:578–564.

Doggett, M. S., and D. Porter. 1996. Sexual reproduction in the

fungal parasite, Zygorhizidium planktonicum. Mycologia

88:720–732.

Doolittle, R. F., D. F. Feng, S. Tsang, G. Cho, and E. Little.

1996. Determining divergence times of the major kingdoms

of living organisms with a protein clock. Science 271:470–

477.

Dore, J., and D. A. Stahl. 1991. Phylogeny of anaerobic rumen

Chytridiomycetes inferred from small subunit ribosomal

RNA sequence comparisons. Can. J. Bot. 69:1964–1971.

Edmonds, R. L., J. K. Agee, and R. I. Gara. 2000. Forest health

and protection. McGraw-Hill Series in Forestry. McGraw-

Hill, Boston.

Eriksson, O. E., H.-O. Baral, R. S. Currah, K. Hansen, C. P.

Kurtzman, G. Rambold, and T. Laessшe. 2003. Pp. 1–89 in

Outline of Ascomycota—2003. Myconet Umeе, Umeе

University. Available: http://www.umu.se/myconet/

Myconet.html. Last accessed 3 December 2003.

Eslava, A. P., and M. I. Alvarez. 1996. Genetics of Phycomyces.

Pp. 385–406 in Fungal genetics: principles and practice

(C. J. Bos, ed.). Marcel Dekker, New York.

Fell, J. W., T. Boekhout, A. Fonseca, and J. P. Sampaio. 2001.

Basidiomycetous yeasts. Pp. 3–35 in The mycota VIIB,

systematics and evolution (D. J. McLaughlin, E. G.

McLaughlin, and P. A. Lemke, eds.). Springer-Verlag, Berlin.

Feng, D. F., G. Cho, and R. F. Doolittle. 1997. Determining

divergence times with a protein clock: update and reevaluation.

Proc. Natl. Acad. Sci. USA 94:13028–13033.

Forget, L., J. Ustinova, Z. Wang, V. A. R. Huss, and B. F. Lang.

2002. The “colorless green alga” Hyaloraphidium curvatum: a

linear mitochondrial genome, tRNA editing, and an

evolutionary link to lower fungi. Mol. Biol. Evol. 19:310–

319.

Fцrster, H., M. D. Coffey, H. Elwood, and M. L. Sogin. 1990.

Sequence analysis of the small subunit ribosomal RNAs of

three zoosporic fungi and implications for fungal evolution.

Mycologia 82:306–312.

Fuller, M. S., and R. E. Reichle. 1968. The fine structure of

Monoblepharella sp. zoospores. Can. J. Bot. 46:279–283.

Gargas, A., P. T. DePriest, M. Grube, and A. Tehler. 1995.

Multiple origins of lichen symbioses in fungi suggested by

SSU rDNA phylogeny. Science 268:1492–1495.

Gehrig, H., A. SchьЯler, and M. Kluge. 1996. Geosiphon

pyriforme, a fungus forming endocytobiosis with Nostoc

(Cyanobacteria), is an ancestral member of the Glomales:

evidence by SSU rRNA analysis. J. Mol. Evol. 43:71–81.

Geiser, D. M., and K. F. LoBuglio. 2001. The monophyletic

Plectomycetes: Ascosphaeriales, Onygenales, Eurotiales.

Pp. 201–219 in The mycota VIIA, systematics and evolution

(D. J. McLaughlin, E. G. McLaughlin, and P. A. Lemke,

eds.). Springer-Verlag, New York.

Gernandt, D. S., J. L. Platt, J. K. Stone, J. W. Spatafora, A. Holst-

Jensen, R. C. Hamelin, and L. M. Kohn. 2001. Phylogenetics

of Helotiales and Rhytismatales based on partial

small subunit nuclear ribosomal DNA sequences. Mycologia

93:915–933.

The Fungi 191

Glass, N. L., and I. A. J. Lorimer. 1991. Ascomycete mating

types. Pp 193–216 in More gene manipulations in fungi

( J. W. Bennett and L. L. Lasure, eds.). Academic Press,

Orlando, FL.

Gottlieb, A. M., and R. W. Lichtwardt. 2001. Molecular variation

within and among species of Harpellales. Mycologia 93:66–

81

Griffin, D. H. 1994. Fungal physiology. 2nd ed. Wiley-Liss,

New York.

Haselwandter, K., O. Bolbleter, and D. J. Read. 1990. Degradation

of 14C-labelled lignin and dehydropolymer of coniferyl

alchohol by ericoid and ectomycorrhizal fungi. Arch.

Microbiol. 153:352–354.

Hawksworth, D. L. 1991. The fungal dimension of biodiversity:

magnitude, significance and conservation. Mycol. Res.

95:641–655.

Hawksworth, D. L. 2001. The magnitude of fungal diversity: the

1.5 million species estimate revisited. Mycol. Res. 105:1422–

1432.

Hawksworth, D. L., P. M. Kirk, B. C. Sutton, and D. N. Pegler.

1995. Ainsworth and Bisby’s dictionary of the fungi. 8th ed.

CAB International, Wallingford, UK.

Heath, I. B., T. Bauchop, and R. A. Skipp. 1983. Assignment of

the rumen anaerobe Neocallimastix frontalis to the Spizellomycetales

(Chytridiomycetes) on the basis of its polyflagellate

ultrastructure. Can. J. Bot. 61:295–307.

Heckman, D. S., D. M. Geiser, B. R. Eidell, R. L. Stauffer, N. L.

Kardos and S. B. Hedges. 2001. Molecular evidence for the

early colonization of land by fungi and plants. Science

293:1129–1133.

Hibbett, D. S., and M. Binder. 2002. Evolution of complex

fruiting body morphologies in homobasidiomycetes. Proc.

R. Soc. Lond. B 269:1963–1969.

Hibbett, D. S., and M. J. Donoghue. 2001. Analysis of character

correlations among wood decay mechanisms, mating

systems, and substrate ranges in homobasidiomycetes. Syst.

Biol. 50:215–242.

Hibbett, D. S., L. B. Gilbert, and M. J. Donoghue. 2000.

Evolutionary instability of ectomycorrhizal symbioses in

basidiomycetes. Nature 407:506–508.

Hibbett, D. S., E. M. Pine, E. Langer, G. Langer, and M. J.

Donoghue. 1997. Evolution of gilled mushrooms and

puffballs inferred from ribosomal DNA sequences. Proc.

Natl. Acad. Sci. USA 94:12002–12006.

Hibbett, D. S., and R. G. Thorn. 2001. Basidiomycota: Homobasidiomycetes.

Pp. 121–168 in The mycota VIIB, systematics

and evolution (D. J. McLaughlin, E. G. McLaughlin, and

P. A. Lemke, eds.). Springer-Verlag, Berlin.

Holst-Jensen, A., L. M. Kohn, and T. Schumacher. 1997.

Nuclear rDNA phylogeny of the Sclerotiniaceae. Mycologia

89:885–899.

Humber, R. A., and K. S. Hansen. USDA-ARS Collection of

Entomopathogenic Fungal Cultures (ARSEF). Available:

http://www.ppru.cornell.edu/mycology/Insect_mycology.

htm. Last accessed 3 December 2003.

Ingold, C. T. 1965. Spore liberation. Clarendon Press, Oxford.

James, T. Y., D. Porter, C. A. Leander, R. Vilgalys, and J. E.

Longcore. 2000. Molecular phylogenetics of the Chytridiomycota

supports the utility of ultrastructural data in chytrid

systematics. Can. J. Bot. 78:336–350.

Jensen, A. B., A. Gargas, J. Eilenberg, and S. Rosendahl. 1998.

Relationships of the insect-pathogenic order Entomophtorales

(Zygomycota, Fungi) based on phylogenetic analyses

of nuclear small subunit ribosomal DNA sequences (SSU

rDNA). Fungal Genet. Biol. 24:325–334.

Karling, J. S. 1977. Chytridiomycetarum Iconographia.

Lubrecht and Cramer, Monticello, NY.

Kauff, F., and F. Lutzoni. 2002. Phylogeny of the Gyalectales

and Ostropales (Ascomycota, Fungi): among and within

order relationships based on nuclear ribosomal RNA

small and large subunits. Mol. Phylogenet. Evol. 25:138–

156.

Keeling, P. J., M. A. Luker, and J. D. Palmer. 2000. Evidence

from beta-tubulin phylogeny that microsporidia evolved

from within the fungi. Mol. Biol. Evol. 17:23–31.

Kirk, P. M., P. F. Cannon, J. C. David, and J. A. Stalpers. 2001.

Ainsworth and Bisby’s dictionary of the fungi. 9th ed. CAB

International, Wallingford, UK.

Klironomos, J. N., and M. M. Hart. 2001. Animal nitrogen swap

for plant carbon. Nature 410:651–652.

Kohlmeyer, J., and E. Kohlmeyer. 1979. Marine mycology. The

higher fungi. Academic Press, New York.

Kurtzman, C. P., and C. J. Robnett. 2003. Phylogenetic

relationships among yeasts of the “Saccharomyces complex”

determined from multigene sequence analyses. FEMS Yeast

Res. 1554:1–16.

Kwon-Chung, K. J., and J. E. Bennett. 1992. Medical mycology.

Lea and Febiger, Philadelphia.

Landvik, S. 1996. Neolecta, a fruit-body-producing genus of the

basal ascomycetes, as shown by SSU and LSU rDNA

sequences. Mycol. Res. 100:199–202.

Landvik, S., O. E. Eriksson, and M. L. Berbee. 2001. Neolecta—

a fungal dinosaur? Evidence from b-tubulin amino acid

sequences. Mycologia 93:1151–1163.

Lang, B. F. 2001. Fungal Mitochondrial Genome Project. Http://

megasun.bch.umontreal.ca/People/lang/FMGP/.

Lang, B. F, C. O’Kelly, T. Nerad, M. W. Gray, and G. Burger.

2002. The closest unicellular relative of animals. Curr. Biol.

12:1773–1778.

Lange, L., and L. W. Olson. 1979. The uniflagellate phycomycete

zoospore. Dansk Bot. Arkiv. 33:7–95.

Li, J., and I. B. Heath. 1992. The phylogenetic relationships of

the anaerobic chytridiomycetous gut fungi (Neocallimasticaceae)

and the Chytridiomycota. I. Cladistic analysis

of rRNA sequences. Can. J. Bot. 70:1738–1746.

Lichtwardt, R. W. 1986. The trichomycetes, fungal associates of

arthropods. Springer-Verlag, New York.

Lichtwardt, R. W., M. J. Cafaro, and M. M. White. 2001. The

Trichomycetes: rev. ed. Available: http://www.nhm.ku.edu/

%7Efungi/monograph/text/mono.htm. Last accessed 3

December 2003.

Liu, Y. J., S. Whelen, and B. D. Hall. 1999. Phylogenetic

relationships among ascomycetes: evidence from an RNA

polymerse II subunit. Mol. Biol. Evol. 16:1799–1808.

Longcore, J. E. 1992. Morphology, occurrence, and zoospore

ultrastructure of Podochytrium dentatum sp. nov.

(Chytridiales). Mycologia 84:183–192.

Longcore, J. E. 1996. Chytridiomycete taxonomy since 1960.

Mycotaxon 60:149–174.

Longcore, J. E., A. P. Pessier, and D. K. Nichols. 1999. Batracho192

The Relationships of Fungi

chytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic

to amphibians. Mycologia 91:219–227.

Loytynoja, A., and M. C. Milinkovitch. 2001. Molecular

phylogenetic analyses of the mitochondrial ADP-ATP

carriers: the Plantae/Fungi/Metazoa trichotomy revisited.

Proc. Natl. Acad. Sci. USA 98:10202–10207.

Luttrell, E. S. 1951. Taxonomy of the Pyrenomycetes. Univ. Mo.

Stud. 24:1–120.

Luttrell, E. S. 1955. The ascostromatic Ascomycetes. Mycologia

47:511–532.

Lutzoni, F., and M. Pagel. 1997. Accelerated evolution as a

consequence of transitions to mutualism. Proc. Nat. Acad.

Sci. USA 94:11422–11427.

Lutzoni, F. L., M. Pagel, and V. Reeb. 2001. Major fungal

lineages are derived from lichen symbiotic ancestors. Nature

411:937–940.

Marsh, L. 1991. Signal transduction during pheromone

response in yeast. Annu. Rev. Cell Biol. 7:699–728.

McKerracher, L. J., and I. B. Heath. 1985. The structure and

cycle of the nucleus-associated organelle in two species of

Basidiobolus. Mycologia 77:412–417.

McLaughlin, D. J., E. G. McLaughlin, and P. A. Lemke. 2001.

The mycota VIIA: systematics and evolution. Springer-

Verlag, New York.

Miadlikowska, J., and F. Lutzoni. In press. Phylogenetic

classification of peltigeralean fungi (Peltigerales,

Ascomycota) based on ribosomal RNA small and large

subunits. Am. J. Bot.

Molina, R., and J. M. Trappe. 1982. Patterns of ectomycorrhizal

host specificity and potential among pacific northwest

conifers and fungi. Forest Sci. 28:423–458.

Moncalvo, J. M., R. Vilgalys, S. A. Redhead, J. E. Johnson, T. Y.

James, M. C. Aime, V. Hofstetter, S. J. W. Verduin, E.

Larsson, T. J. Baroni, et al. 2002. One hundred and

seventeen clades of Euagarics. Mol. Phylogenet. Evol.

23:357–400.

Nagahama, T., H. Sato, M. Shimazu, and J. Sugiyama. 1995.

Phylogenetic divergence of the entomophthoralean fungi:

evidence from nuclear 18s ribosomal RNA gene sequence.

Mycologia 87:203–209.

Nash, T. H. 1996, Lichen biology. Cambridge University Press,

Cambridge.

Nishida, H., K. Ando, Y. Ando, A. Hirata, and J. Sugiyama.

1995. Mixia osmundae: transfer from the Ascomycota to the

Basidiomycota based on evidence from molecules and

morphology. Can. J. Bot. 73:S660–S666.

Nishida, H., and J. Sugiyama. 1994. Archiascomycetes:

detection of a major new linage within the Ascomycota.

Mycoscience 35:361–366.

Nyvall, P., M. Pedersйn, and J. E. Longcore. 1999. Thalassochytrium

gracilariopsidis (Chytridiomycota), gen. et sp.

nov., endosymbiotic in Gracilariopsis sp. (Rhodophyceae).

J. Phycol. 35:176–185.

Oberwinkler, F. 1977. Das neue System der Basidiomyceten.

Pp. 59–105 in Biologie der niederen Pflanzen (H. Frey,

H. Hurka, and F. Oberwinkler, eds.). G. Fischer, Stuttgart.

O’Donnell, K. 1979. Zygomycetes in culture. Department of

Botany, University of Georgia, Athens.

O’Donnell, K., E. Cigelnik, and G. L. Benny. 1998. Phylogenetic

relationships among the Harpellales and Kickxellales.

Mycologia 90:624–639.

O’Donnell, K., F. M. Lutzoni, T. J. Ward, and G. L. Benny.

2001. Evolutionary relationships among mucoralean fungi

(Zygomycota): evidence for family polyphyly on a large

scale. Mycologia 93:286–296.

Orpin, C. G. 1988. Nutrition and biochemistry of anaerobic

Chytridiomycetes. Biosystems 21:365–370.

Paquin, B., M.-J. Laforest, L. Forget, I. Roewer, Z. Wang,

J. Longcore, and F. Lang. 1997. The fungal mitochondrial

genome project: evolution of fungal mitochondrial genomes

and their gene expression. Curr. Genet. 31:380–395.

Perez-Moreno, J., and D. J. Read. 2000. Mobilization and

transfer of nutrients from litter to tree seedlings via the

vegetative mycelium of ectomycorrhizal plants. New Phytol.

145:301–309.

Pirozynski, K. A., and D. W. Malloch. 1975. The origin of land

plants: a matter of mycotropism. Biosystems 6:153–164.

Platt, J. L., and J. W. Spatafora. 2000. Evolutionary relationships

of nonsexual lichenized fungi: molecular phylogenetic

hypotheses for the genera Siphula and Thamnolia from SSU

and LSU rDNA. Mycologia 92:475–487.

Powell, M. J. 1978. Phylogenetic implications of the microbodylipid

globule complex in zoosporic fungi. Biosystems

10:167–180.

Powell, M. J. 1993. Looking at mycology with a Janus face: a

glimpse at Chytridiomycetes active in the environment.

Mycologia 85:1–20.

Powell, M. J., and W. J. Koch. 1977. Morphological variations

in a new species of Entophlyctis. II. Influence of

growth conditions on morphology. Can. J. Bot. 55:1686–

1695.

Prillinger, H., F. Oberwinkler, C. Umile, K. Tlachac, R. Bauer,

C. Dцrfler, and E. Taufratzhofer. 1993. Analysis of cell wall

carbohydrates (neutral sugars) from ascomycetous and

basidiomycetous yeasts with and without derivatization.

J. Gen. Appl. Microbiol. 39:1–34.

Raju, N. B. 1992. Genetic control of the sexual cycle in

Neurospora. Mycol. Res. 96:241–262.

Rayner, A. D. M., and L. Boddy. 1988. Fungal decomposition of

wood: its biology and ecology. John Wiley, Chichester, UK.

Redecker, D., R. Kodner, and L. E. Graham. 2000a. Glomalean

fungi from the Ordovician. Science 289:1920–1021.

Redecker, D., J. B. Morton, and T. D. Bruns. 2000b. Ancestral

lineages of arbuscular mycorrhizal fungi (Glomales). Mol.

Phylogenet. Evol. 14:276–284.

Reid, I. D. 1995. Biodegradation of lignin. Can. J. Bot. 73:S1011–

S1018.

Remy, W., T. N. Taylor, and H. Hass. 1994a. Early Devonian

fungi—a Blastocladalean fungus with sexual reproduction.

Am. J. Bot. 81:690–702.

Remy, W., T. N. Taylor, H. Hass, and H. Kerp. 1994b.

4–Hundred-million-year-old vesicular-arbuscular mycorrhizae.

Proc. Natl. Acad. Sci. USA 91:11841–11843.

Rinaldi, M. G. 1989. Zygomycosis. Infect. Dis. Clin. N. Am.

3:19–41.

Roane, M. K., and R. A. Paterson. 1974. Some aspects of

morphology and development in the Chytridiales.

Mycologia 66:147–164.

The Fungi 193

Sanders, I. R. 1999. No sex please, we’re fungi. Nature 399:737–

739.

Sanderson, M. J. 2002. Estimating absolute rates of molecular

evolution and divergence times: a penalized likelihood

approach. Mol. Biol. Evol. 19:101–109.

SchьЯler, A., D. Schwarzott, and C. Walker. 2001. A new fungal

phylum, the Glomeromycota: phylogeny and evolution.

Mycol. Res. 105:1413–1421.

Schwarzott, D., C. Walker, and A. SchьЯler. 2001. Glomus,

the largest genus of the arbuscular mycorrhizal Fungi

(Glomales), is nonmonophyletic. Mol. Phylogenet. Evol.

21:190–197.

Selosse, M. A., and F. Le Tacon. 1998. The land flora: a

phototroph-fungus partnership? Trends Ecol. Evol. 13:15–

20.

Sherwood-Pike, M. A., and J. Gray. 1985. Silurian fungal

remains: probable records of the Class Ascomycetes. Lethaia

18:1–20.

Simon, L., J. Bousquet, R. C. Lйvesque, and M. Lalonde. 1993.

Origin and diversification of endomycorrhizal fungi and

coincidence with vascular land plants. Nature 363:67–69.

Sjamsuridzal, W., H. Nishida, H. Ogawa, M. Kakishima, and

J. Sugiyama. 1999. Phylogenetic positions of rust fungi

parasitic on ferns: evidence from 18S rDNA sequence

analysis. Mycoscience 40:21–27.

Smith, M. L., J. N. Bruhn, and J. B. Anderson. 1992. The fungus

Armillaria bulbosa is among the largest and oldest living

organisms. Nature 356:428–434.

Smith, S. E., and D. J. Read. 1997. Mycorrhizal symbiosis.

Academic Press, San Diego.

Sparrow, F. K. 1960. Aquatic phycomycetes. 2nd rev. ed.

University of Michigan Press, Ann Arbor.

Spatafora, J. W. 1995. Ascomal evolution among filamentous

ascomycetes: evidence from molecular data. Can. J. Bot.

S811–S815.

Spatafora, J. W., and M. Blackwell. 1994. The polyphyletic

origins of ophiostomatoid fungi. Mycol. Res. 98:1–9.

Spatafora, J. W., B. Volkmann-Kohlmeyer, and J. Kohlmeyer.

1998. Independent terrestrial origins of the Halosphaeriales

(marine Ascomycota). Am. J. Bot. 85:1569–1580.

Sugiyama, J. 1987. Pleomorphic fungi: the diversity and its

taxonomic implications. Elsevier, Amsterdam.

Suh, S.-O., and M. Blackwell. 1999. Molecular phylogeny of the

cleistothecial fungi placed in Cephalothecaceae and

Pseudeurotiaceae. Mycologia 91:836–848.

Suh, S.-O., C. Marshall, J. V. McHugh, and M. Blackwell.

2003. Wood ingestion by passalid beetles in the presence

of xylose-fermenting gut yeasts. Mol. Ecol. 12:3137–

3145.

Swann, E. C., E. M. Frieders, and D. J. McLaughlin. 1999.

Microbotryum, Kriegeria and the changing paradigm in

basidiomycete classification. Mycologia 91:51–66.

Swann, E. C., E. M. Frieders, and D. J. McLaughlin. 2001.

Urediniomycetes. Pp. 37–56 in The mycota VIIB, systematics

and evolution (D. J. McLaughlin, E. G. McLaughlin, and

P. A. Lemke, eds.). Springer-Verlag, Berlin.

Swann, E. C., and J. W. Taylor. 1993. Higher taxa of basidiomycetes:

an 18S rRNA gene perspective. Mycologia

85:923–936.

Swann, E. C., and J. W. Taylor. 1995. Phylogenetic perspectives

on basidiomycete systematics: evidence from the 18S rRNA

gene. Can. J. Bot. 73:S862–S868.

Tanabe, Y., K. O’Donnell, M. Saikawa, and J. Sugiyama.

2000. Molecular phylogeny of parasitic Zygomycota

(Dimargaritales, Zoopagales) based on nuclear small

subunit ribosomal DNA sequences. Mol. Phylogenet. Evol.

16:253–262.

Tanabe, Y., Watanabe, M. M., and J. Sugiyama. 2002. Are

Microsporidia really related to fungi? A reappriasal based on

additional gene sequenc es from basal fungi. Mycol. Res.

106:1380–1391.

Taylor, J. W. 1995. Making the Deuteromycota redundant: a

practical integration of mitosporic and meiosporic fungi.

Can. J. Bot. 73:S754–S759.

Taylor, J. W., B. Bowman, M. L. Berbee, and T. J. White.

1993. Fungal model organisms: phylogenetics of Saccharomyces,

Aspergillus and Neurospora. Syst. Biol. 42:440–

457.

Taylor, J. W., and M. S. Fuller. 1981. The Golgi apparatus,

zoosporogenesis, and development of the zoospore

discharge apparatus of Chytridium confervae. Exp. Mycol.

5:35–59.

Taylor, T. N., H. Hass, and H. Kerp. 1997. A cyanolichen from

the Lower Devonian Rhynie Chert. Am. J. Bot. 84:992–

1004.

Taylor, T. N., T. Hass, and H. Kerp. 1999. The oldest fossil

ascomycetes. Nature 399:648–648.

Taylor, T. N., H. Hass, W. Remy, and H. Kerp. 1995a. The

oldest fossil lichen. Nature 378:244–244.

Taylor, T. N., W. Remy, and H. Hass. 1992. Fungi from the

Lower Devonian Rhynie Chert—Chytridiomycetes. Am. J.

Bot. 79:1233–1241.

Taylor, T. N., W. Remy, and H. Hass. 1994. Allomyces in the

Devonian. Nature 367:601–601.

Taylor, T. N., W. Remy, H. Hass, and H. Kerp. 1995b. Fossil

arbuscular mycorrhizae from the Early Devonian. Mycologia

87:560–573.

Taylor, T. N., and E. L. Taylor. 1997. The distribution and

interactions of some Paleozoic fungi. Rev. Palaeobot.

Palynol. 95:83–94.

Tehler, A., J. S. Farris, D. L. Lipscomb, and M. Kдllersjo. 2000.

Phylogenetic analyses of the fungi based on large rDNA data

sets. Mycologia 92:459–474.

Thorn, R. G., and G. L. Barron. 1984. Carnivorous mushrooms.

Science 224:76–78.

Ustinova, I., L. Krienitz, and V. A. R. Huss. 2000. Hyaloraphidium

curvatum is not a green alga, but a lower fungus; Amoebidium

parasiticum is not a fungus, but a member of the DRIPs.

Protist 151:253–262.

Varma, A., and B. Hock. 1999. Mycorrhiza: structure, function,

molecular biology, biotechnology. Springer-Verlag, New

York.

Vogler, D. R., and T. D. Bruns. 1998. Phylogenetic relationships

among the pine stem rust fungi (Cronartium and Peridermium

spp.). Mycologia 90:244–257.

Wainright, P. O., G. Hinkle, M. L. Sogin, and S. K. Stickel.

1993. Monophyletic origins of the Metazoa: “an evolutionary

link with fungi.” Science 260:340–342.

194 The Relationships of Fungi

Wang, D. Y. C., S. Kumar, and S. B. Hedges. 1999. Divergence

time estimates for the early history of animal phyla and the

origin of plants, animals and fungi. Proc. R. Soc. Lond. B

266:163–171.

Wasson, G. 1980. The wondrous mushroom: mycolatry in

Mesoamerica. McGraw-Hill, New York.

Weir, A., and M. Blackwell. 2001. Molecular data support

the Laboulbeniales as a separate class of Ascomycota,

Laboulbeniomycetes. Mycol. Res. 105:715–722.

Wells, K., and R. J. Bandoni. 2001. Heterobasidiomycetes.

Pp. 85–120 in The mycota VIIB, systematics and evolution

(D. J. McLaughlin, E. G. McLaughlin, and P. A. Lemke,

eds.). Springer-Verlag, Berlin.

Wessels, J. G. H. 1994. Developmental regulation of fungal cell

wall formation. Annu. Rev. Phytopathol. 32:413–437.

Wu, C. G., and J. W. Kimbrough. 1992. Ultrastructural studies

of ascosporogenesis in Ascobolus immersus. Mycologia

84:459–466.

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