In textbooks published before 1990, extant angiosperms were consistently subdivided into two major groups – dicotyledons (dicots) and monocotyledons (monocots), based partly on the number of cotyledons in the seedling. This dichotomy was long considered to represent a fundamental divergence at the base of the angiosperm evolutionary tree. Other features marked this distinction, including the absence of a vascular cambium and presence of parallel leaf venation in monocots. However, the expansion of molecular phylogenetics through the early 1990s indicated that some species that were formerly classified as primitive dicots do not belong to either category, though the monophyly of monocots was confirmed. Thus, although the dicot/monocot distinction remains useful for generalized descriptions of angiosperm groups, current evidence suggests that it does not represent a wholly natural classification. It is now widely accepted that several relatively species-poor angiosperm lineages (here termed early-divergent angiosperms or magnoliids) evolved before the divergence of the two major lineages that led to the monocots and the remaining dicots (now termed eudicots, or sometimes tricolpates).

Early-divergent angiosperms (including magnoliids) are a small but highly diverse assemblage of taxonomically isolated lineages that probably represent the surviving extant members of their respective clades, accounting for only about 1% of extant species.

Introduction

The Plasmodiophoromycota are a group of obligate (i.e. biotrophic) parasites. The best-known examples attack higher plants, causing economically significant diseases such as club-root of brassicas (Plasmodiophora brassicae), powdery scab of potato (Spongospora subterranea; formerly S. subterranea f. sp. subterranea) and crook-root disease of watercress (S. nasturtii; formerly S. subterranea f. sp. nasturtii). In addition to damaging crops directly, some species (S. subterranea, Polymyxa betae, P. graminis) also act as vectors for important plant viruses (Adams, 1991; Campbell, 1996). Other species infect roots and shoots of non-cultivated plants, especially aquatic plants. Algae, diatoms and Oomycota are also attacked. If the nine species of Haptoglossa, which parasitize nematodes and rotifers, are included in the Plasmodiophoromycota, the phylum currently comprises 12 genera and 51 species (Dick, 2001a). Genera are separated from each other largely by the arrangement of resting spores in the host cell (Waterhouse, 1973). This feature has also been used for naming most genera; for instance, in Polymyxa, numerous resting spores are contained within each sorus, whereas in Spongospora the resting spores are grouped loosely in a sponge-like sorus (Fig. 3.6). Accounts of the Plasmodiophoromycota have been given by Sparrow (1960), Karling (1968), Dylewski (1990) and Braselton (1995, 2001).

Taxonomic considerations

Plasmodiophoromycota have traditionally been studied by mycologists and plant pathologists. Many general features of their biology and epidemiology are similar to those of certain members of the Chytridiomycota such as Olpidium (see p. 145).

Throughout this book we have attempted to consider fungi showing predominantly or purely asexual reproduction together with their known or suspected teleomorphs. However, certain groups of taxonomically diverse fungi colonizing the same specialized habitats or substrates are best understood in their ecological context, especially if they show strikingly similar adaptations and morphology despite their different evolutionary histories. Two cases illustrating such convergent evolution among anamorphic fungi are the nematophagous habit and the aquatic habitat, which we shall consider in turn in this chapter.

Nematophagous fungi

Nematodes are a very varied group of invertebrates. They are particularly common as free-living saprotrophic species in the soil, around plant roots, on dung and in all kinds of decomposing plant matter, as well as in freshwater and marine habitats. Most saprotrophic nematodes feed on bacteria, although fungal hyphae may also be consumed. Other species parasitize animals, releasing their eggs or motile stages into the environment when their hosts defaecate. Plant-parasitic species chiefly attack roots as free-living or sedentary organisms. Sedentary species form adult stages inside plant root tissues where they cause the economically important root knot diseases (Meloidogyne spp.) or root cyst diseases (Heterodera spp. and Globodera spp.). Plant-parasitic nematodes are readily recognized because their mouth parts are modified as stylets with which they penetrate plant tissues. Gravid females of cyst nematodes enlarge, and their bodies become converted into a hardened cyst containing the eggs.

Introduction

The class Heterobasidiomycetes is approximately synonymous with the terms ‘Phragmobasidiomycetes’ or ‘jelly fungi’ and contains fungi with the following characteristics.

1. The dolipore septum is complex, i.e. it is surrounded by a parenthesome. Parenthesomes are also found in the Homobasidiomycetes (Chapters 19 and 20), but not in the Urediniomycetes (Chapter 22) and Ustilaginomycetes (Chapter 23).

2. The basidia of Heterobasidiomycetes may be strongly lobed and often divided by transverse, oblique or longitudinal septa. Such basidia are loosely termed heterobasidia, especially if they arise directly from hyphae instead of teliospores as in most Urediniomycetes and Ustilaginomycetes. If the basidia are septate, they are also called phragmobasidia. The sterigma of the heterobasidium is unusually prominent and is often termed epibasidium (Martin, 1945). In contrast, the basidia of Homobasidiomycetes are club-shaped and always single-celled.

3. The fruit bodies of most Heterobasidiomycetes are simpler in architecture than those of Homobasidiomycetes, and the hymenium is not normally protected by a roof- or shelf-like architecture. In compensation, these simple fruit bodies are generally able to survive drying and rehydration, with fresh crops of basidiospores produced after each rehydration event. Fully hydrated basidiocarps are typically greatly swollen and gelatinous, hence the term ‘jelly fungi’ for the Heterobasidiomycetes.

4. The basidiospores of most species are capable of producing secondary spores which may be ballistoconidia, passively released conidia or yeast cells.

Species included in this class show considerable morphological diversity, and taxonomic concepts have been in a state of flux.

Introduction

The class Hemiascomycetes contains the classical ascomycete yeasts, exclusive of those which belong to the Archiascomycetes (see the preceding chapter) and the ‘black yeasts’ such as Aureobasidium (see p. 486). Detailed descriptions of the individual yeast genera and species are given in Kurtzman and Fell (1998) and Barnett et al. (2000). A useful taxonomic overview is that by Kurtzman and Sugiyama (2001). There is only one order, the Saccharomycetales, which has been divided into 11 families and 276 species (Kirk et al., 2001; Kurtzman & Sugiyama, 2001). However, detailed phylogenetic analyses of the Hemiascomycetes (Kurtzman & Robnett, 1998, 2003) indicate that this family arrangement is likely to be modified in the future, and for this reason we shall focus on selected genera.

The key feature that distinguishes the Hemi- and Archiascomycetes from the higher ascomycetes (Euascomycetes) is that ascogenous hyphae and an ascocarp, i.e. an investment of sterile hyphae surrounding the asci, are lacking in the first two groups. Instead, the asci are formed freely and singly, either directly following karyogamy or more rarely after a prolonged diploid phase. Another distinguishing feature is the composition of the cell wall, which contains very little chitin in the Hemi- and Archiascomycetes. Chitin is often confined to a small ring around the site where the daughter cell is produced (the bud scar). An ultrastructural feature of distinction concerns the septal pore of any hypha that may be produced.

Introduction

When the first slime moulds were described by Johann H. F. Link in 1833, they were given the term myxomycetes (Gr. myxa = slime). Link used the suffix -mycetes because of the superficial similarity of the fructifications of slime moulds with the fruit bodies of certain fungi, notably Gasteromycetes (see Chapter 20). Although it has been appreciated for some time that they lack any true relationship with the Eumycota (de Bary, 1887; Whittaker, 1969), slime moulds have none the less been studied mainly by mycologists rather than protozoologists, probably because they occur in the same habitats as fungi and are routinely encountered during fungus forays. Since slime moulds are only rarely covered by zoology courses even today, they are briefly described in this chapter, referring to more specialized literature as appropriate.

Slime moulds differ substantially from the Eumycota not only in phylogenetic terms, but also regarding their physiology and ecology. Their vegetative state is that of individual amoebae in the cellular slime moulds, or of a multinuclear (coenocytic) plasmodium in the plasmodial slime moulds. Motile stages bearing usually two anterior whiplash-type flagella may be present in the plasmodial slime moulds (Sections 2.4, 2.5) and in the Plasmodiophoromycota (Chapter 3). Amoebae or plasmodia feed by the ingestion (phagocytosis) of bacteria, yeast cells or other amoebae. This is followed by intracellular digestion in vacuoles. The mode of nutrition in slime moulds is therefore fundamentally different from extracellular degradation and absorption as shown by Eumycota.

Introduction

The phylum Chytridiomycota comprises over 900 species in five orders (D. J. S. Barr, 2001; Kirk et al., 2001). Fungi included here are colloquially called ‘chytrids’. Most chytrids grow aerobically in soil, mud or water and reproduce by zoospores with a single posterior flagellum of the whiplash type, although the zoospores of some members of the Neocallimastigales are multiflagellate. Some species inhabit estuaries and others the sea. Sparrow (1960) has given an extensive account of aquatic forms, Karling (1977) a compendium of illustrations, and Powell (1993) has provided examples of the importance of the group. Many members are saprotrophs, utilizing cellulose, chitin, keratin, etc., from decaying plant and animal debris in soil and mud, whilst species of Caulochytrium grow as mycoparasites on the mycelium and conidia of terrestrial fungi (Voos, 1969). Saprotrophs can be obtained in crude culture by floating baits such as cellophane, hair, shrimp exoskeleton, boiled grass leaves and pollen on the surface of water overlying samples of soil, mud or pieces of aquatic plant material (Sparrow, 1960; Stevens, 1974; Willoughby, 2001). From such crude material, pure cultures may be prepared by streaking or pipetting zoospores onto agar containing suitable nutrients and antibiotics to limit contamination from bacteria. The growth and appearance of chytrids in pure culture is variable and often differs significantly from their natural habit. This has led to problems in classification systems based on thallus morphology (Barr, 1990, 2001). The availability of cultures has, however, facilitated studies on chytrid nutrition and physiology (Gleason, 1976).

Introduction

The dual nature of lichens was first hinted at by de Bary (1866) and clearly recognized by Schwendener (1867). A lichen is now defined as a ‘self-supporting association of a fungus (mycobiont) and a green alga or cyanobacterium (photobiont)’ (Kirk et al., 2001), ‘resulting in a stable thallus of specific structure’ (Ahmadjian, 1993). The fungal partner usually contributes most of the biomass to this symbiosis, including the external surface. It is thus termed the exhabitant, whereas the unicellular or filamentous photobiont cells are collectively called the inhabitant because they are located inside the lichen thallus (see Ahmadjian, 1993). Most lichens have a characteristic appearance which permits their identification if suitable keys are available (e.g. Purvis et al., 1992; Wirth, 1995a, b; Brodo et al., 2001). Since the structure of lichens is almost entirely due to the fungal partner, lichen taxonomy is synonymous with the taxonomy of the mycobiont.

It is possible to grow the algal and fungal partners of many lichens separately in pure culture (Ahmadjian, 1993; Crittenden et al., 1995). Whereas most photobionts multiply readily in pure culture, the fungal partner, if it grows at all, typically shows slow growth as a sterile leathery mycelium but does not produce the characteristic lichen thallus. This is in marked contrast to the natural thallus where the mycobiont displays its full sexual and asexual cycle, whereas the photobiont cells often appear swollen and are arrested in their cell cycle, i.e. their cell division is controlled by the mycobiont.

Introduction

The kingdom Chromista was erected by Cavalier-Smith (1981, 1986) to accommodate eukaryotic organisms which are distinguishable from the Protozoa by a combination of characters. Some of these are concerned with details of photosynthesis, such as the enclosure of chloroplasts in sheets of endoplasmic reticulum, and the absence of chlorophyll b, the latter feature being used for the naming of the kingdom. Other defining characters apply also to the non-photosynthetic members of the Chromista (Kirk et al., 2001). These are as follows:

1. The structural cell wall polymer is cellulose, in contrast to walls of Eumycota which contain chitin.

2. The inner mitochondrial membrane is folded into tubular cristae (Fig. 4.1a) which are also found in plants. In contrast, mitochondrial cristae are generally lamellate in the kingdoms Eumycota (Fig. 4.1b) and Animalia.

3. Golgi stacks (dictyosomes) are present; these are also found in the Protozoa (see p. 64). In contrast, in the Eumycota the Golgi apparatus is usually reduced to single cisternae (see Figs. 1.3, 1.10).

4. Flagella are usually present during particular stages of the life cycle; they always include one straminipilous flagellum (Lat. stramen = straw, pilus = hair). Dick (2001a) considered this feature to be of such high phylogenetic significance that he has renamed the kingdom Chromista as Straminipila. The straminipilous flagellum is discussed in detail in the following section.

5. The amino acid lysine is synthesized via the α,ε-diaminopimelic acid (DAP) pathway.

There are several available good textbooks of mycology, and some justification is needed for publishing another. I have long been convinced that the best way to teach mycology, and indeed all biology, is to make use, wherever possible, of living material. Fortunately with fungi, provided one chooses the right time of the year, a wealth of material is readily available. Also by use of cultures and by infecting material of plant pathogens in the glasshouse or by maintaining pathological plots in the garden, it is possible to produce material at almost any time. I have therefore tried to write an introduction to fungi which are easily available in the living state, and have tried to give some indication of where they can be obtained. In this way I hope to encourage students to go into the field and look for fungi themselves. The best way to begin is to go with an expert, or to attend a Fungus Foray such as those organized in the spring and autumn by mycological and biological societies. I owe much of my own mycological education to such friendly gatherings. A second aim has been to produce original illustrations of the kind that a student could make for himself from simple preparations of living material, and to illustrate things which he can verify for himself. For this reason I have chosen not to use electron micrographs, but to make drawings based on them.

Ustilaginomycetes

The Ustilaginomycetes are one of the four main classes of Basidiomycota and contain about 1500 species (Kirk et al., 2001). In its present form as circumscribed by Begerow et al. (1997) and Bauer et al. (1997, 2001), this group is monophyletic. Hypha-producing Ustilaginomycetes are united by their lifestyle as ecologically obligate plant pathogens, often with an additional free-living (saprotrophic) yeast phase. They can be distinguished from the rust fungi in that haustoria are either altogether absent or, where present, take the shape of simple intracellular hyphae or hyphal extensions which invaginate the host plasmalemma but are not differentiated into a narrow neck and a wider haustorial body. Further, intracellular hyphae of Ustilaginomycetes usually secrete a thick sheath which is readily visible by transmission electron microscopy (see Figs. 23.6 and 23.17). The septa either lack perforations or contain simple pores or dolipores which are similar to those in the Urediniomycetes in lacking parenthesomes. True clamp connections are not usually found. The basidia of smut fungi produce numerous basidiospores whereas those of rust fungi usually produce only four.

The class Ustilaginomycetes has been divided into three subclasses by Begerow et al. (1997, 2000). We shall consider representatives of two of these. The Ustilaginomycetidae (Section 23.2) are the most important plant-pathogenic Ustilaginomycetes, causing smut-like symptoms. Typical members of the Exobasidiomycetidae (Section 23.4) cause other biotrophic diseases and are distinguished from the former by producing basidia directly from parasitic mycelium, not from teliospores.

Introduction

The Pyrenomycetes are defined here according to Samuels and Blackwell (2001) as fungi which produce non-fissitunicate or occasionally prototunicate asci usually in flask-shaped ascomata (perithecia), less frequently in cleistothecia. The sub-class Pyrenomycetes is one of several groups belonging to the huge and heterogeneous class Hymenoascomycetes. The characteristic feature of this class is that the asci develop in an ascohymenial way, i.e. the ascoma is formed after plasmogamy and the pairing of nuclei have occurred, and the asci therefore arise from a hymenium. This is in contrast to asci being formed singly (Archiascomycetes, Hemiascomycetes), scattered throughout the fruit body (Plectomycetes), or formed in a locule within a pre-formed fruit body (Loculoascomycetes). Although the term ‘Pyrenomycetes’ is not generally understood in a taxonomic sense at the present, Samuels and Blackwell (2001) pointed out the monophyly of a core group of orders, including all those which we shall describe in this chapter (summarized in Table 12.1).

The development of the perithecium follows several different schemes defined by Luttrell (1951), which are described in more detail for the different orders. Following fertilization and plasmogamy, the ascogonium gives rise to ascogenous hyphae while the perithecial wall is formed by hyphae arising from the ascogonial stalk or elsewhere. Sterile hyphae growing up from the basal fertile region (paraphyses) and periphyses which line the inner surface of the ostiole, may be present. The development of the opening of the perithecium is typically schizogenous, i.e.

Introduction

The phylum Zygomycota comprises the first group of fungi considered in this book which lacks any motile stage. Asexual reproduction is by spores which are called aplanospores because they are non-motile, and sporangiospores because they are typically contained within sporangia. They are dispersed passively by wind, insects and rain splash, although violent liberation of entire sporangia (e.g. Pilobolus) or individual spores (e.g. Basidiobolus, Entomophthora) can also occur. Sexual reproduction is by gametangial copulation which is typically isogamous and results in the formation of a zygospore. The mycelial organization is coenocytic, and the cell wall contains chitin and its deacetylated derivative, chitosan (Bartnicki-Garcia, 1968, 1987; see Fig. 1.5). As in the Chytridio-, Asco- and Basidiomycota, the mitochondria possess lamellate cristae, and the Golgi system is reduced to single cisternae. Lysine is synthesized by the α-aminoadipic acid (AAA) route, as it appears to be in all Eumycota.

General accounts of the Zygomycota have been given by Benjamin (1979), Benny (2001) and Benny et al. (2001). Molecular evidence indicates that the group may have diverged from the Chytridiomycota early in the history of terrestrial life. The Zygomycota, in turn, probably gave rise to the Asco- and Basidiomycota, i.e. the ‘higher fungi’ (Jensen et al., 1998; Schüssler et al., 2001). Two classes are included in the Zygomycota, namely Zygomycetes comprising 870 species in 10 orders, and Trichomycetes with 218 species in 3 orders (Kirk et al., 2001). The most prominent orders of the Zygomycetes are the Mucorales, Entomophthorales and Glomales.

Introduction

Several independent phylogenetic analyses of DNA sequence data (e.g. Berbee & Taylor, 1993; Sjamsuridzal et al., 1997; Liu & Hall, 2004) have grouped together a range of seemingly very diverse genera of ascomycetes. This group is considered to be the oldest of three broad evolutionary lineages of Ascomycota and has thus been named Archiascomycetes (Nishida & Sugiyama, 1994). The core of the Archiascomycetes consists of the genera Taphrina and Protomyces, which are facultative biotrophic plant pathogens, and the saprotrophic fission yeast Schizosaccharomyces. Also now included are the yeast-like Pneumocystis, which causes pneumonia in immunocompromised patients (see p. 259); the filamentous fungus Neolecta, which parasitizes the roots of higher plants (Redhead, 1977; Landvik et al., 2003); and the anamorphic yeast Saitoella. Yet other genera are included as possible members because even though their appropriate DNA sequences have not yet been obtained, they are known to be related to confirmed members. In total, the class Archiascomycetes currently contains some 150 species in 10 genera.

Because of their diverse morphological appearances and modes of life, it is difficult to describe common characters typical of the Archiascomycetes. With the exception of Neolecta, which produces apothecia, ascocarps are lacking and asci are produced individually by yeast cells or by conversion of hyphal tips. There are no differentiated ascogenous hyphae. Asexual reproduction is usually by simple division of vegetative yeast cells by budding or fission.

In revising the first edition, which was first published about ten years ago, I have taken the opportunity to give a more complete account of the Myxomycota, and to give a more general introduction to the Eumycota. An account has also been given of some conidial fungi, as exemplified by aquatic Fungi Imperfecti, nematophagous fungi and seed-borne fungi. The taxonomic framework has been based on Volumes IVA and IVB of Ainsworth, Sparrow and Sussman's The Fungi: An Advanced Treatise (Academic Press, 1973).