Introduction To Fungi
Carris, L.M., C.R. Little and C.M. Stiles. 2012. Introduction to Fungi. The Plant Health Instructor. DOI:10.1094/PHI-I-2012-xxxx
Lori M. Carris, Christopher R. Little and Carol M. Stiles
Washington State University, Kansas State University, and Georgia Military College
What is a fungus?
A fungus is a eukaryote that digests food externally and absorbs nutrients directly through its cell walls. Most fungi reproduce by spores and have a body (thallus) composed of microscopic tubular cells called hyphae. Fungi are heterotrophs and, like animals, obtain their carbon and energy from other organisms. Some fungi obtain their nutrients from a living host (plant or animal) and are called biotrophs; others obtain their nutrients from dead plants or animals and are called saprotrophs (saprophytes, saprobes). Some fungi infect a living host, but kill host cells in order to obtain their nutrients; these are called necrotrophs.
Fungi were once considered to be primitive members of the plant kingdom, just slightly more advanced than bacteria. We now know that fungi are not primitive at all. In fact, recent taxonomic treatments such as the Tree of Life Project show that fungi and animals both belong to the group Opisthokonta (Fig. 1). Fungi may not be our next of kin, but they are more closely related to animals than they are to plants. We also recognize that organisms traditionally studied as “fungi” belong to three very different unrelated groups: the true fungi in Kingdom Fungi (Eumycota), the Oomycetes, and the slime molds (Fig. 1).
Let’s briefly consider the major groups in Kingdom Fungi—they will be described in greater detail later. Open most introductory mycology books and you’ll see that there are four main groups (phyla) of true fungi—Ascomycota, Basidiomycota, Chytridiomycota and Zygomycota (e.g., Alexopoulos et al. 1996; Webster and Weber 2007). Recent studies have provided support for the recognition of additional phyla, such as Glomeromycota, a group of fungi once placed in Zygomycota that form an association with the roots of most plants (Fig. 2). A group of parasitic organisms called Microsporidia that live inside the cells of animals are also now considered to belong in the fungal kingdom (Fig. 2). Hibbett et al. (2007) published a comprehensive classification of the Kingdom Fungi, the result of collaboration among many fungal taxonomists. This classification is used in the Dictionary of the Fungi (Kirk et al. 2008) and other fungal references and databases. However, the classification system will undergo additional changes as scientists use new methods to study the fungi. For example, Jones et al. (2011) described the “cryptomycota,” a potentially new phylum of organisms within the Kingdom Fungi.
How old are fungi?
Fungi are an ancient group—not as old as bacteria, which fossil evidence suggests may be 3.5 billion years old—but the earliest fungal fossils are from the Ordovician, 460 to 455 million years old (Redecker et al. 2000). Based on fossil evidence, the earliest vascular land plants didn’t appear until approximately 425 million years ago, and some scientists believe that fungi may have played an essential role in the colonization of land by these early plants (Redeker et al. 2000). Mushrooms exquisitely preserved in amber from the Late Cretaceous (94 million years ago) tell us that there were mushroom-forming fungi remarkably similar to those that exist today when dinosaurs were roaming the planet (Hibbett et al. 2003). However, the fungal fossil record is incomplete and provides only a minimum time estimate for when different groups of fungi evolved. Molecular data suggest that fungi are much older than indicated by the fossil record, and may have arisen more than one billion years ago (Parfrey et al. 2011).
How many fungi are there?
No one knows for sure how many species of fungi there are on our planet at this point in time, but what is known is that at least 99,000 species of fungi have been described, and new species are described at the rate of approximately 1200 per year (Blackwell 2011; Kirk et al. 2008). A conservative estimate of the total number of fungal species thought to exist is 1.5 million (Hawksworth 2001). To come up with this figure, Hawksworth estimated the known numbers of plant and fungal species from countries in which both plants and fungi have been well-studied—Great Britain and Ireland, in this case—and determined there were six fungal species for every native plant species. The total number of plant species worldwide is approximately 250,000, and if the ratio of fungi to plants in Great Britain is typical of what occurs elsewhere, there should be at least 1.5 million species of fungi (6 × 250,000; Hawksworth 2001).
If 1.5 million fungal species is a reasonable estimate, the vast majority of all extant fungi are yet to be named. Assuming a relatively constant rate at which new species are described, it will take more than 1100 years to catalog and describe all remaining fungi. However, many of these fungi are likely to become extinct before they are ever discovered given current rates of habitat and host loss. For example, up to 2% of tropical forests are destroyed globally each year (Purvis and Hector 2000). These habitats are exceedingly rich in fungal species (Hawksworth and Rossman 1997). For example, 15-25% of fungi collected in short-term studies in the tropics are new species (Kirk et al. 2008). Callan and Carris (2004) estimated that an 110,000 ha neotropical forest, such as in Costa Rica, could contain over 81,000 different species of plant parasitic fungi—almost as many as all the known species of fungi! Consider that this estimate was based only on plant parasitic fungi, and did not take into account other ecological groups of fungi such as saprotrophs.
What do fungi do?
Fungi are involved in a wide range of activities—some fungi are decomposers, parasites or pathogens of other organisms, and others are beneficial partners in symbiosis with animals, plants or algae. Let’s take a brief look at these various ecological groups.
Fungi associated with animals
Fungi have the ability to grow on and in both invertebrate and vertebrate animals. Many fungi can attack insects and nematodes, for example, and may play an important role in keeping populations of these animals under control. Insect-attacking fungi, called "entomopathogens," include a wide range of fungi in phyla Ascomycota, Zygomycota and Chytridiomycota. Some of the best-known and most spectacular entomopathogens belong in the Ascomycota genus Ophiocordyceps and related genera. These fungi infect and consume insects such as caterpillars and ants, and then form conspicuous stromata that emerge from their victim’s body in a most dramatic manner (Fig. 3). These fungi can also alter the insect’s behavior. “Zombie-ant” fungi from Brazil infect insect brains, directing the victim to climb up plants and bite into the plant tissue in a “death grip” (Evans et al. 2011; Hughes et al. 2011). Paradoxically, humans have been using one of these entomopathogens, Ophiocordyceps sinensis, for thousands of years to treat a wide range of ailments. This fungus is an important component of traditional Asian medicine (Fig. 3) and is commonly called “winter worm, summer grass.”
Entomopathogens such as Beauveria bassiana are so effective in killing insects that they are used as biological control agents for insect pests. Colony collapse disorder of honeybees has been associated with co-infection by a virus and a microsporidian fungus, Nosema ceranae (Bromenshenk et al. 2010). One group of fungi called Entomophthorales ("insect killers") includes a number of highly specialized entomopathogens. A common example is Entomophthora musae, which is often observed forming a ring of white spores discharged around the body of a parasitized fly on panes of glass.
Some fungi are specialized parasites of nematodes, rotifers, and other microscopic animals in the soil (Barron 1977). A common nematode predator is Arthrobotrys oligospora, a fungus that has evolved sticky networks of hyphae for trapping nematodes. Once the nematode is immobilized, the fungus invades and consumes its body.
Fortunately, there are relatively few fungal pathogens of vertebrates—only 200-300 species—but some of these fungi can have devastating impacts. Consider the well-publicized frog killer, Batrachochytrium dendrobatidis, a member of phylum Chytridiomycota (Berger et al. 1998; Longcore et al. 1999). This fungus wasn’t even known to scientists until 1996, when it was discovered associated with frogs that had died from a mysterious skin disease at the Smithsonian National Zoological Park in Washington, D.C. The fungus doesn’t invade the frog’s body, but it is lethal, possibly because it disrupts electrolyte balance leading to cardiac arrest (Voyles et al. 2009)—infected frogs appear to die of a heart attack! The frog chytrid is implicated in the widespread decline of frog populations around the world. Fortunately, this is the only chytrid known to parasitize a vertebrate animal and it appears to infect only amphibians.
Another devastating parasite of animals is Geomyces destructans, a cold-loving fungus that causes ‘white-nose syndrome’ in bats (Blehert et al., 2009). This fungus colonizes the skin on the muzzles, ears and wing membranes of some types of bats, and infected bats exhibit unusual behavior. The bat fungus is associated with declines in bat populations in the northeastern U.S. and has many wildlife biologists concerned. As of 2011, white-nose syndrome had been confirmed in 16 states and four Canadian provinces.
In humans, there are several different types of fungal infections, or "mycoses." The most common are caused by dermatophytes, fungi that colonize dead keratinized tissue including skin, finger-, and toenails. Dermatophytes cause superficial infections such as ‘ringworm’ that are unsightly and difficult to treat, but rarely serious. Some fungi are members of the resident microflora in healthy people, but become pathogenic in people with predisposing conditions. For example, Candida species cause annoying yeast infections in the mucosal tissues of many healthy people, but can also cause diseases collectively called candidiasis in babies and immunocompromised individuals. Another group of fungi are inhaled as spores and initiate infection through the lungs. These fungi include Coccidioides immitis (coccidioidomycosis, commonly known as valley fever), and Histoplasma capsulatum (histoplasmosis). Opportunistic fungal pathogens are normally not associated with humans and other animals, but can cause serious infections in weakened or healthy individuals when inhaled or implanted in wounds. Aspergillus fumigatus, one of the most important of these opportunists, produces small, airborne spores that are frequently inhaled; in some individuals the fungus starts growing invasively, causing a disease known as aspergillosis, especially in immunocompromised individuals.
A remarkable discovery was that Pneumocystis carinii, the organism causing pneumonia-like symptoms in immunocompromised patients, is a fungus and not a protozoan as had been thought for decades. Why was this pathogen classified as a protozoan? It does not respond to the common drugs used to treat fungal infections, but does respond to anti-protozoan drugs. This unusual fungus emerged as one of the leading causes of death in AIDS patients in the late twentieth century.
Fungi and plants
The association of fungi and plants is ancient and involves many different fungi. Fungi are an important group of plant pathogens—most plant diseases are caused by fungi—but fewer than 10% of all known fungi can colonize living plants (Knogge, 1996). Plant pathogenic fungi represent a relatively small subset of those fungi that are associated with plants. Most fungi are decomposers, utilizing the remains of plants and other organisms as their food source. Other types of associations that will be discussed here include the role of fungi as decomposers, as beneficial symbionts, and as cryptic plant colonizers called endophytes.
Most fungi are associated with plants as saprotrophs and decomposers. These fungi break down organic matter of all kinds, including wood and other types of plant material. Wood is composed primarily of cellulose, hemicellulose, and lignin. Lignin is a complex polymer that is highly resistant to degradation, and it encrusts the more readily degradable cellulose and hemicellulose. Fungi are among the few organisms that can effectively break down wood, and fall into two main types—brown and white rot fungi. Brown rot fungi selectively degrade the cellulose and hemicellulose in wood, leaving behind the more recalcitrant lignin. The decayed wood is brown in color and tends to form cubical cracks due to the brittle nature of the remaining lignin (Fig. 4). Only ~10% of the wood decay fungi cause brown rot, and most of these fungi (80%) occur on conifer wood. Brown rot residues make up ‘humus’ in temperate forest soils and are important for mycorrhizal formation (see the following paragraph for information on mycorrhizal fungi), moisture retention, and for sequestering carbon. Brown rot residues are highly resistant to decomposition and can remain in the soil for up to 300 years. White rot fungi are more common than brown rot fungi; these fungi degrade cellulose, hemicellulose, and lignin at approximately equal rates. The decayed wood is pale in color, light in weight, and has a stringy texture (Fig. 5). White rot fungi are the only organisms that can completely degrade lignin. Lignin is one of the most abundant organic polymers, accounting for 30% of the organic carbon on the planet—only cellulose is more abundant (Boerjan et al. 2003).
An important group of fungi associated with plants is mycorrhizal fungi. Mycorrhiza means ‘fungus root’, and it refers to a mutually beneficial association (a type of symbiosis) between fungi and plant roots. There are seven major types of mycorrhizal associations, the most common of which is the arbuscular mycorrhizae, involving members of phylum Glomeromycota associated with roots of most major groups of plants. The vast majority (>80%) of vascular plants form mycorrhizae, as will be discussed later (under Glomeromycota).
Another common type of association is ectomycorrhizae formed between forest trees and members of phyla Basidiomycota and Ascomycota. In this association, the fungus forms hyphae around host root cortical cells—the "Hartig net"— and a sheath of hyphae around the host roots called a "mantle." Many of the ectomycorrhizal fungi are mushroom-forming species including highly prized edibles such as chanterelles (Cantharellus cibarius and related species), boletes (Boletus edulis and related species), and matsutake (Tricholoma magnivelare) (Fig. 6). A valuable group of ectomycorrhizal fungi are truffles, members of phylum Ascomycota that form underground fruiting bodies. The French Périgord truffle, Tuber melanospora, and the Italian white truffle, Tuber magnatum, can bring phenomenal prices; for example, a 1.5-kg Italian white truffle sold for $330,000 at an auction in 2007!
Lichens are examples of a symbiotic association involving a fungus and green algae or less frequently Cyanobacteria. The lichen thallus is composed mostly of fungal hyphae, usually with the alga or cyanobacterium confined to discrete areas of the thallus. In lichens, reproductive structures of the fungus are often conspicuous, for example disc- or cup-like structures called apothecia (Fig. 7). The fungus obtains carbohydrates produced by photosynthesis from the algae or cyanobacteria, and in return provides its partner(s) with protection from desiccation and ultraviolet light. Lichens grow in a wide range of habitats on nearly every continent. Think about an inhospitable place, and there’s probably a lichen that grows there—on bare rocks, sidewalks, grave stones, the exoskeletons of some insects, and even on cars that remain for a long time in one place!
Some fungi are hidden inside their plant hosts; these are endophytes, defined by their presence inside asymptomatic plants. All plants in natural ecosystems probably have some type of symbiotic association with endophytic fungi (Rodriguez et al. 2009). Endophytic fungi have been shown to confer stress tolerance to their host plant, for example, to disease, herbivory, drought, heat, salt and metals. The clavicipitaceous endophytes in the genus Neotyphodium (phylum Ascomycota) are among the best studied. These fungi produce alkaloid compounds that protect the grass host from insects that would otherwise feed on them; endophyte-infected turfgrass seed is sold commercially for seeding lawns and other types of grassy recreational areas. Unfortunately, livestock such as sheep, cattle, llamas and horses also are negatively affected by toxins produced by endophytes when they eat infected grass. ‘Ryegrass staggers’ occurs when animals graze on perennial ryegrass (Lolium perenne) that is colonized by Neotyphodium lolii. Afflicted animals develop symptoms including tremors and jerky or uncoordinated movements.
Let’s now consider the role of fungi as plant pathogens. There are thousands of species of plant pathogenic fungi that collectively are responsible for 70% of all known plant diseases. Plant pathogenic fungi are parasites, but not all plant parasitic fungi are pathogens. What is the difference between a parasite and a pathogen? Plant parasitic fungi obtain nutrients from a living plant host, but the plant host doesn’t necessarily exhibit any symptoms. In this sense, endophytic fungi discussed in the preceding paragraph are plant parasites because they live in intimate association with plants and depend on them for nutrition. Plant pathogenic fungi are parasites and cause disease characterized by symptoms.
Biotrophic fungal pathogens obtain nutrients from living host tissues, often via specialized cells called haustoria that form inside host cells (Fig. 8). Necrotrophic pathogens obtain nutrients from dead host tissue, which they kill through the production of toxins or enzymes. Most biotrophic fungi have fairly narrow host ranges—they are specialized on a limited number of plant hosts. Necrotrophic fungi can be either generalists, growing on a wide range of host species, or specialized on a restricted range of hosts. Some plant pathogenic fungi change the way that their hosts grow, either by affecting the level of growth regulators produced by the plant, or by producing growth regulators themselves. Examples of changes in plant growth caused by plant pathogenic fungi include cankers, galls, witches’ broom, leaf curl and stunting.
We can further divide plant pathogenic fungi by the stage of the plant host that is attacked, for example, seeds, seedlings, or adult plants, and by what part of the plant is affected—roots, leaves, shoots, stems, woody tissues, fruits or flowers. A group of fungi including species of Fusarium, Rhizoctonia and Sclerotium cause seed rot and infect plants at the seedling stage. These pathogens can attack a wide range of plants. Often, seedling pathogens cause damping-off symptoms because they occur in wet soils.
Many of the same fungi that kill seedlings can also infect the roots of mature plants and cause root and crown rot diseases. Infection often occurs through wounds, and results in lesions or death of part or all of the root system and crown. Some common root rots of trees are caused by members of phylum Basidiomycota in the genera Armillaria and Heterobasidion. Armillaria spp. produce shoe-string-like bundles of hyphae called rhizomorphs that allow the fungus to grow from one tree to another. Species of Heterobasidion survive as saprotrophs in dead tree stumps and roots, but can also infect living hosts through root contact. These fungi cause decay in the roots and crown; infected trees become weakened and die, or may blow over in high winds. Wood rot fungi, most of which are also members of Basidiomycota, infect trees through wounds, branch stubs and roots, and decay the inner heartwood of living trees. Extensive decay weakens the tree, and reduces the quality of wood in trees harvested for timber (see the discussion of "white rot" and "brown rot" fungi above).
Vascular wilt pathogens kill their host by infecting through the roots or through wounds and growing into the xylem, where they produce small spores that get carried upward until they are trapped at the perforated ends of the xylem vessels. The spores germinate and grow through the pores. The fungus is transported throughout the plant in this manner. The first symptom of vascular wilt is a loss of turgidity in the plant leaves, often on one side of the plant or a single branch. If the stems of infected plants are cut open, vascular discoloration is evident. Among the important vascular wilt fungi are Fusarium oxysporum, Verticillium albo-atrum and V. dahliae.
One of the most famous vascular wilts is Panama disease of bananas, caused by Fusarium oxysporum forma specialis (f.sp.) cubense. This fungus nearly wiped out banana production in Latin America in the early twentieth century. Most bananas that were being grown for export were a single cultivar, 'Gros Michel', which turned out to be highly susceptible to Panama disease. There is no effective method for controlling Panama disease and it rapidly spread throughout banana plantations around the world. The banana industry was saved by the discovery of the cultivar 'Cavendish' that is resistant to the strain of Panama disease that killed 'Gros Michel'. 'Cavendish' is now the banana that Americans and Europeans consume, but a new strain of the Panama disease pathogen began killing 'Cavendish' in Malaysia in 1985 and scientists are concerned that this strain will begin to spread (Ploetz, 2005).
Leaf spot pathogens infect through natural plant openings such as stomates or by penetrating directly through the host cuticle and epidermal cell wall. In order to penetrate directly, fungi produce hydrolytic enzymes—cutinases, cellulases, pectinases and proteases—for breaking down the host tissue. Alternatively, some fungi form specialized structures called appressoria (sing. appressorium) at the end of germ tubes. Turgor pressure builds up in the appressorium, and in combination with an infection peg, mechanical force is exerted to breach the host cell walls. Once inside the plant leaf, the fungus must obtain nutrients from the cells, and this is often accomplished by killing host cells (necrotrophs). Death of host cells is evident as an area of dead cells called a lesion (Fig. 9).
Many leaf-spotting fungi produce toxins that kill host cells and this often produces a lesion surrounded by a yellow halo (Fig. 10). If enough of the leaf surface is killed, or if the infected leaves drop prematurely, the plant’s ability to produce photosynthates is severely impaired.
Returning to bananas, another devastating disease of this host is black leaf streak, or black Sigatoka, caused by Mycosphaerella fijiensis. Unlike the root-infecting pathogen that causes Panama disease, the black Sigatoka pathogen can be controlled by applications of a protective fungicide to banana leaves. Effective control of black Sigatoka requires multiple fungicide applications and control of this disease accounts for up to 25% of the total production cost for bananas (Ploetz, 2001).
American chestnut trees were once a prominent hardwood tree in the eastern U.S., but have largely been eliminated by the chestnut blight pathogen, Cryphonectria parasitica, an example of a canker-causing fungal pathogen. Cankers develop when the pathogen kills the phloem and vascular cambium in a woody host. If the canker encircles the trunk or branch of a tree, that plant part will die. The canker-causing fungus can often be identified based on the fruiting bodies that form in the canker. In contrast to cankers, galls result from abnormal growth of a plant, usually due to an increase in cell size and cell division. Although galls are often associated with insect pests, some fungal pathogens induce galls; two common examples are the black knot pathogen, Apiosporina morbosa on Prunus spp. (Fig. 11), and species of Gymnosporangium, which induce the formation of galls on their coniferous hosts (Fig. 12).
Gymnosporangium is a type of rust fungus. Rust fungi are biotrophic pathogens—they infect, grow, and sporulate in living plant tissue. Even though biotrophs require living host tissue for their growth and reproduction, they can be devastating pathogens by reducing the photosynthetic surface and increasing water loss in the host plant. Rust fungi attack a wide range of plants, and often require two, unrelated hosts in order to complete their life cycles. Rust fungi are so-named because of the abundant orange spores that are formed on plants that are infected by these fungi; infected plants often look as though they are rusting.
One historically important rust fungus is black stem rust of wheat, a disease that was well known to the ancient Romans. Black stem rust, caused by Puccinia graminis f.sp. tritici, infects wheat and barberry (Berberis species). Since the barberry host is required for the pathogen to complete its life cycle, early control measures in the United States and Canada were aimed at eliminating this host, not the economically important host, wheat. We now know that this method of eradication was of limited success because rust spores can be carried long distances—for example, from northern Mexico to the U.S.-Canada border—by wind currents via the "Puccinia pathway” (Nagarajan and Singh 1990).