Morphological characteristics of fungi: mycelium and hyphae
Now let’s take a closer look at fungi and the types of structures that they form. A key characteristic of fungi that has contributed to their successful exploitation of diverse ecological niches is the formation of a filamentous thallus called the mycelium. A mycelium is composed of branching, microscopic tubular cells called hyphae (Fig. 13) that grow through and across substrates or food sources, secreting enzymes that break down complex substrates into simple compounds that can be absorbed back through the cell wall. The fungal cell wall in the Kingdom Fungi is composed of chitin and glucans (in Ascomycota, Basidiomycota and Chytridiomycota) as well as chitosan and other components (in Zygomycota) (Kirk et al., 2008)
Hyphae can have cross walls called septa, or lack cross walls (nonseptate; aseptate; coenocytic). The type of hyphae—septate or aseptate—is characteristic of specific groups of fungi. In fungi that form septate hyphae, there are perforations at the septa, called septal pores, which allow the movement of cytoplasm and organelles from one compartment to the next. The type and complexity of the septal pore is characteristic of specific groups of fungi.
Hyphae grow from a germinating spore or other type of propagule, and these are described in more detail in the section “Fungal Reproduction.” Hyphae elongate almost exclusively at the tips, growing outwards from the point of establishment. As a result of apical growth, hyphae are relatively uniform in diameter, and mycelium that grows in an unimpeded manner forms a circular colony on solid substrates that support fungal growth; agar, a gelatinous material derived from seaweed, amended with different types of nutrients is commonly used to grow fungi in culture (Fig. 14).
Some fungi grow exclusively or mostly as yeasts, defined as single-celled fungi that reproduce by budding or fission. In contrast to apical growth that is characteristic of hyphae, yeasts exhibit wall growth over the entire cell surface, often resulting in a nearly spherical cell (Fig. 15). There are also fungi that can switch between mycelial growth and yeast-like growth, dependent upon the environmental conditions. The ability to grow in different forms is called dimorphism, and is exhibited by some members of phyla Ascomycota, Basidiomycota and Zygomycota.
Inside the fungal cell
Most of the organelles present in fungal cells are similar to those of other eukaryotes. Fungal nuclei are usually small (< 2 µm diameter), and can compress and/or stretch to move through septal pores and into developing spores. Fungi have been found to possess between 6 and 21 chromosomes coding for 6,000 to nearly 18,000 genes. Genome sizes range from 8.5 megabase pairs (Mb) to just over 400 Mb in filamentous fungi (Zolan 1995; Spanu et al. 2010; Duplessis et al. 2011), making fungal genomes among the smallest of eukaryotic organisms on average—approximately 1% the size of mammalian genomes and only 1.3 times the size of the largest known bacterial genome (Stover et al. 2000). Many fungi (Ascomycota) have a life cycle that is predominantly haploid, while others (Basidiomycota) have a long dikaryotic phase.
Fungi frequently reproduce by the formation of spores. A spore is a survival or dispersal unit, consisting of one or a few cells, that is capable of germinating to produce a new hypha. Unlike plant seeds, fungal spores lack an embryo, but contain food reserves needed for germination. Many fungi produce more than one type of spore as part of their life cycles. Fungal spores may be formed via an asexual process involving only mitosis (mitospores), or via a sexual process involving meiosis (meiospores). The manner in which meiospores are formed reflects the evolutionary history and thus the classification for the major groups (phyla) of fungi.
Many fungi produce spores inside or upon a fruiting body. Many people are familiar with the mushroom, a type of fruiting body produced by some Basidiomycota. You may recognize other fungal fruiting bodies such as puffballs, or shelf fungi. These are examples of large, conspicuous fruiting bodies, but there is an even greater diversity of microscopic fruiting bodies produced by various fungi. What all fruiting bodies have in common is that they produce spores and provide a mechanism for dispersing those spores. Fruiting bodies will be discussed in more detail within the fungal groups.
Teleomorph and anamorph
Many fungi are able to reproduce by both sexual and asexual processes. Sexual and asexual reproduction may require different sets of conditions (e.g., nutrients, temperature, light, moisture). In some fungi, two sexually compatible strains must conjugate (mate) in order for sexual reproduction to occur. The terms ‘anamorph’ and ‘teleomorph’ are used to convey the asexual and sexual reproduction morphological types, respectively, in a particular fungus. The concept of anamorph and teleomorph is a confusing one for many students, as we are not accustomed to thinking about organisms with such reproductive flexibility. For a more thorough discussion of anamorph and teleomorph, refer to Alexopoulos et al. (1996), Kendrick (2000), or Webster and Weber (2007).
Examples of meiospores—spores that are the products of meiosis—include ascospores (see Ascomycota) and basidiospores (see Basidiomycota). Ascospores are formed inside a sac-like structure called an ascus (Fig. 16). An ascus starts out as a sac of cytoplasm and nuclei, and by a process called "free cell formation" (Kirk et al. 2008) a cell wall forms de novo around each nucleus and surrounding cytoplasm to form ascospores (typically eight per ascus). Ascospores vary in size, shape, color, septation, and ornamentation among taxa. Basidiospores are formed on a basidium (Fig. 17) and are typically one-celled with one or two haploid nuclei. Basidiospores vary in size, color and ornamentation depending upon the taxonomic group. More information on dispersal of ascospores and basidiospores can be found below.
Examples of mitospores are conidia (sing. conidium), sporangiospores, and zoospores, formed by members of the phyla Ascomycota, Zygomycota, and Chytridiomycota, respectively. Another type of asexual propagule produced by fungi in several different phyla is the chlamydospore.
Conidia are formed from a modified hypha or a differentiated conidiogenous cell of the fungus. Conidiogenous cells can be formed singly on hyphae, on the surface of aggregated hyphal structures, or within different types of fruiting bodies. Fruiting bodies inside which conidia are formed are pycnidia and acervuli. Sporodochia and synnemata are examples of fruiting bodies on which conidia are formed. Conidia are produced primarily by Ascomycota, although some Basidiomycota are capable of producing them as well.
Sporangiospores are asexual propagules formed inside a globose or cylindrical sporangium by a process involving cleavage of the cytoplasm. Sporangiospores are thin-walled, one-celled, hyaline or pale-colored, and are usually globose or ellipsoid in shape. One to 50,000 sporangiospores may be formed in a single sporangium. When mature, sporangiospores are released by breakdown of the sporangial wall, or the entire sporangium may be dispersed as a unit. Sporangiospores are produced by fungi in phyla Chytridiomycota and Zygomycota, as well fungal-like Oomycetes (see section “Fungal-like Organisms Studied by Plant Pathologists and Mycologists”).
A zoospore is a microscopic, motile propagule, approx. 2 to 14 µm long and 2 to 6 µm in diameter that lacks a cell wall and is characterized by having one or more flagella. Flagella are ~ 0.25 µm in diameter and up to 50 µm long. Zoospores are produced by one group of true Fungi (Chytridiomycota), and by fungal-like organisms in Kingdom Straminipila and some slime molds (see section “Fungal-like Organisms Studied by Plant Pathologists and Mycologists”). Two types of flagella are known—the whiplash flagellum, which is directed backward, and the tinsel flagellum, which is directed forward. The tinsel flagellum is only present in members of Kingdom Straminipila and does not occur in true fungi. The length of time zoospores are able to swim is determined by their endogenous energy reserves—zoospores cannot obtain food from external sources—and environmental conditions. Zoospores may exhibit chemotaxis—movement in response to a chemical gradient, e.g., root exudates. At the end of its motile phase, the zoospore undergoes a process called encystment in which it either sheds or retracts the flagella and produces a cell wall. The encysted zoospore, called a cyst, may germinate directly by the formation of a germ tube, or indirectly by the emergence of another zoospore.
Zoospores are formed inside a sac-like structure called a zoosporangium by a process involving mitosis and cytoplasmic cleavage—similar to the formation of sporangiospores in sporangia. Depending upon the taxonomic group, zoospores emerge from the zoosporangium through breakdown of the zoosporangial wall, through a preformed opening in the wall covered with a cap called an operculum that flips back, or by a gelatinous plug that dissolves.
Chamydospores are survival propagules formed from an existing hyphal cell or a conidium that develops a thickened wall and cytoplasm packed with lipid reserves. The thickened cell walls may be pigmented or hyaline, and chlamydospores develop singly or in clusters, depending upon the fungus. Chlamydospores are passively dispersed, in most instances when the mycelium breaks down. Chlamydospores are formed by many different groups of fungi and are often found in aging cultures.
Sclerotia (sing. sclerotium) are compact aggregations of hyphae differentiated into an outer, pigmented rind, and an inner mass of hyaline cells called a medulla. Sclerotia contain food reserves, and are a type of survival propagule produced by a number of fungi in phyla Ascomycota and Basidiomycota; in some fungi, such as Rhizoctonia solani, they are the only type of propagule produced, whereas in fungi such as Claviceps purpurea and Sclerotinia sclerotiorum, they are overwintering structures that can germinate directly, or give rise to structures in which the meiospores are formed.
The characteristics and diversity of the major phyla of true Fungi will be briefly described. Selected representatives of the different phyla are introduced and, in many instances, illustrated. A generalized life cycle also is presented for each phylum that illustrates when plasmogamy (cell fusion), karyogamy (nuclear fusion) and meiosis occur relative to each other, and the types of structures involved in these events. For more detailed information on members of Kingdom Fungi, recommended reading is provided at the end of this article.
Phylum Ascomycota is the largest group of fungi, with approximately 33,000 described species in three subphyla—Taphrinomycotina, Saccharomycotina, and Pezizomycotina. Members of this phylum reproduce sexually or meiotically (Fig. 18 – general life cycle) via production of ascospores inside a sac-like structure called an ascus (Fig. 19).
Many species of Ascomycota also (or exclusively) produce spores through an asexual or mitotic process; these spores, called conidia, exhibit a wide range of size, shape, color and septation among the different fungi in which they are formed. Conidia and ascospores are usually produced at different times of year, if ascospores are formed in the lifecycle. The existence of many Ascomycota having sexual and asexual states that are separated in time and space has long confused those new to mycology and plant pathology. The asexual states of Ascomycota are especially important to the plant pathologist because they are more commonly encountered than the sexual state, and must be identified for control, quarantine, or other purposes. Fungi that reproduce only via asexual means have been given various designations including deuteromycetes, fungi imperfecti, mitosporic fungi, conidial fungi, and anamorphic fungi.
Subphylum Taphrinomycotina includes fungi that, with one known exception, do not form fruiting bodies—as examples, the fission yeast Schizosaccharomyces (Fig. 20), plant parasites in the genera Protomyces and Taphrina (peach leaf curl; see Figs. 21 & 22), and Pneumocystis, a yeast-like fungus previously mentioned (in “Fungi associated with animals”) that causes pneumonia in animals including humans.
Subphylum Saccharomycotina contains approximately 1500 species of yeasts, most of which live as saprotrophs in association with plants and animals, but also including a small number of plant and animal pathogens (Suh et al. 2006). Asci are formed naked (Fig. 23)—not enclosed in a fruiting body. Yeasts traditionally have been important in the production of beer, wine, single cell protein and baker’s yeast, but their role in industry has expanded to the production of citric acid, fuel alcohol, and riboflavin (Kurtzman and Sugiyama 2001). Saccharomyces cerevisiae (Fig. 15), the yeast used in baking and brewing, is an important model organism for scientists studying a wide range of genetic and physiological processes. In 1997, S. cerevisiae was the first eukaryotic organism to have its genome completely sequenced.
Subphylum Pezizomycotina is the largest group in the phylum, with more than 32,000 identified species that occupy a wide range of ecological niches, occurring as saprotrophs, parasites and mutualists with plants, animals and other fungi. At least 40% of the species form lichens (Fig. 24). Three different types of asci occur in this subphylum, prototunicate, unitunicate and bitunicate. Prototunicate asci release ascospores by breakdown of the ascus wall, whereas in the unitunicate and bitunicate asci, the ascospores are forcibly discharged. Bitunicate asci have an inner wall that balloons out from the outer wall prior to ascospore discharge, and in unitunicate asci the wall layers do not separate from each other. A wide range of fruiting bodies are formed by members of subphylum Pezizomycotina, including cleistothecia, chasmothecia, apothecia, perithecia and pseudothecia. Stromata, hardened masses of hyphae on or in which perithecia or pseudothecia are formed, occur in some members of this subphylum.
Cleistothecia (sing. cleisothecium) (Fig. 25) lack a preformed opening and ascospores are released by the breakdown of the ascomatal wall. Common fungi that produce cleistothecia include the teleomorphic (sexual) states of Aspergillus and Penicillium (Fig. 26). Species of Aspergillus are important in the production of fermented foods and beverages, including soy sauce, miso and rice wine (sake). Some species of Aspergillus infect animals, causing a disease known as aspergillosis, and others produce mycotoxins. Aflatoxin is a potent carcinogen produced by A. flavus that occurs in food made from cereals, corn and peanuts that have been colonized by the fungus. The U.S. Food and Drug Administration established a strict limit of 20 parts per billion on aflatoxin levels in food, and the U.S. spends $30-50 million annually on aflatoxin testing (Robens & Cardwell 2003). Penicillium species are also used in food production. For example, the blue veins in Roquefort and Gorgonzola cheeses are due to the growth and sporulation of particular species of Penicillium (Fig. 27), as is the white rind on the outside of Camembert cheese. The antibiotic penicillin, the "wonder drug" of the 20th century, is produced by strains of P. chrysogenum (Raper, 1978). Other species of Penicillium, such as P. digitatum and P. italicum cause the blue and green molds commonly causing rots of citrus fruits.
Chasmothecia (sing. chasmothecium) also lack a preformed opening, but ascospores are released by a split (or “chasm”) in the ascomatal wall (Fig. 28). The term is now used to refer to the fruiting bodies of the powdery mildew fungi (Fig. 29) in order Erysiphales.
Apothecia (sing. apothecium) are exposed, often cup-shaped fruiting bodies (Fig. 30), but can take on a variety of forms, including those found in the morels (Morchella spp. Fig. 31). Apothecia-forming fungi are also called “cup fungi” or discomycetes. Some important groups of plant pathogens that form apothecia include species of Monilinia (brown rot of peach; Figs. 32 & 33), and Sclerotinia.
Perithecia (sing. perithecium) are enclosed ascomata with a preformed opening (ostiole) through which ascospores are discharged (Fig. 34). Most fungi producing perithecia also have unitunicate asci and are classified in Sordariomycetes, one of the largest classes of Ascomycota with more than 3,000 described species (Zhang et al. 2006). These fungi have also been called pyrenomycetes. Members of this group are common in nearly all ecosystems, where they occur as saprotrophs, endophytes of plants, or pathogens of plants, animals and other fungi. A large number of economically important plant pathogens belong to Sordariomycetes, including those that cause anthracnose diseases (Glomerella cingulata), blasts (Magnaporthe oryzae, rice blast pathogen), blights (Cryphonectria parasitica, chestnut blight), ergot (Claviceps purpurea), and Fusarium head blight (scab) of small grains (Gibberella zeae).
Pseudothecia (sing. pseudothecium) look similar to perithecia, but they differ in development. Asci form in locules (openings) inside vegetative fungal tissue called ascostroma; this group has been called loculoascomycetes, but is now placed in class Dothideomycetes. Other characteristics of Dothideomycetes include the formation of bitunicate asci, and many members of this group produce darkly pigmented, multiseptate asospores or conidia. Similar to the Sordariomycetes, members of Dothideomycetes occur in a wide range of habitats as saprotrophs and associate with plants as pathogens, endophytes and growing on the surface of plants as epiphytes (Schoch et al. 2006). Examples of well-known plant pathogens belonging to this group include Venturia inaequalis (apple scab; Fig. 35) and Mycosphaerella fijiensis (Black Sigatoka disease of banana); some of the common asexually reproducing fungi that belong in Dothideomycetes are Alternaria (Fig. 36), Cladosporium (Fig. 37), Phoma, and Stemphylium.
Most of the lichen-forming members of Ascomycota belong in class Lecanoromycetes. This is the largest class of fungi, with over 13,500 described species (Miadlikowska et al. 2006). Most of the members of this class produce apothecial fruiting bodies (Figs. 7, 24, 38, 39). The majority of lichenized fungi form a symbiotic association with green algae, and approximately 10% are associated with cyanobacteria. The lichen thallus produces a wide range of secondary metabolites that are of biological and ecological importance (Miadlikowska et al. 2006). The lichen thallus is able to grow under a range of adverse conditions and some can survive for hundreds of years. Lichens are found in a wide range of habitats from the Arctic to Antarctic, including some species that can grow in aquatic and marine environments (Webster and Weber 2007).
Phylum Basidiomycota represents the second largest phylum of fungi, with nearly 30,000 described species. Members of phylum Basidiomycota produce basidiospores on a typically club-shaped structure called a basidium (Fig. 17). Characteristic of the mycelium of many members of Basidiomycota is the presence of clamp connections (Figs. 40 & 41) and dolipore septa.
Three main lineages are recognized in phylum Basidiomycota: subphyla Ustilaginomycotina, Pucciniomycotina, and Agaricomycotina (Blackwell et al. 2006). Ustilaginomycotina and Pucciniomycotina are composed mostly of plant parasitic species, known as smut and rust fungi, respectively, characterized by a state that produces thick-walled teliospores (Figs. 42 & 43). The most extensively studied members of Ustilaginomycotina are species of Tilletia and Ustilago. Ustilago maydis, which causes corn smut (Fig. 44), produces conspicuous tumor-like growths on infected host plants. These structures eventually become filled with dark teliospores and are considered a delicacy in Mexico called “cuitlacoche.” The most economically important species of Tilletia are the wheat bunts (T. caries and T. laevis—common bunt; T. contraversa—dwarf bunt; and T. indica—Karnal bunt), plant pathogens that convert host ovaries into masses of dark, thick-walled teliospores that smell like rotting fish (Fig. 45).
Subphylum Pucciniomycotina include the group of plant parasites called rust fungi. The rust fungi are remarkable in having as many as five distinct types of spores in a single life cycle (spermatia, aeciospores, urediniospores, teliospores, and basidiospores) (Fig. 46 – general life cycle). Rust fungi that produce all five spore states are macrocyclic, those that do not form uredinospores are demicyclic, and those that do not form urediniospores and aeciospores are microcyclic. Rust fungi may complete the life cycle on one host (autoecious rusts) or require two unrelated alternate hosts for completion of the life cycle (heteroecious rusts). The most widely cited example of a macrocyclic, heteroecious rust is Puccinia graminis (black stem rust), which forms two spore states (uredinia and telia) on cultivated wheat (Fig. 47) and two different spore states (spermagonia and aecia) on barberry leaves (Fig. 48). The fifth state, the probasidium producing basidiospores, is formed upon germination of the teliospores (Fig. 46).
Subphylum Agaricomycotina, previously known as the Hymenomycetes, includes the morphologically diverse group of fungi that produce basidia in various types of fruiting bodies (Fig. 49 – general life cycle). This group includes the fungi commonly known as mushrooms (Fig. 50), puffballs (Fig. 51), shelf fungi (Fig. 52), stinkhorns (Fig. 53), jelly fungi (Figs. 54 & 55) and bird’s nest fungi (Fig. 56). Many species are saprotrophic, utilizing dead plant material including woody substrates. Some of these saprotrophic species are cultivated for food, for example, the common button mushroom (Agaricus bisporus), oyster mushrooms (Pleurotus ostreatus), and shiitake (Lentinula edodes). Other members of this group are important ectomycorrhizal fungi, forming mutualistic associations with the roots of a wide range of trees. Some fruiting bodies produced by ectomycorrhizae are considered choice edibles, for example, chanterelles (Cantharellus cibarius and other species), porcini (Boletus edulis), and the American matsutake (Tricholoma magnivelare) (Fig. 6). A few members of this group are economically important plant parasites, e.g., species of Armillaria and Rhizoctonia.