Introduction to Mycology in the Tropics

2 Introduction to the Fungi and Fungus Like Organisms S approx. 100,000 Fungi and fungus-like organisms are investigated within the scope of the scientific area known as mycology (Gr. mykes = fungus; Gr. logos = discourse). In ancient times, “mykes” referred to fungi with a cap and a stipe, but in the course of time the concept changed, and now all fungi are included.

Systematics: In the past, fungi were considered to be plants and their investigation was conducted

within botany, together with other “lower” plants. Many mushrooms grow from the soil like plants, and most fungi are immobile.

Fungi, however, differ fundamentally from plants by not being able to photosynthesize sugars. Fungi are heterotrophic organisms like animals. Today, we know that true fungi (kingdom Fungi) and animals are more closely related to each other than true fungi are to plants (Fig. 2.1).

FIGURE 2.1. A simplified phylogeny, including fungi and pseudofungi (names written in bold) and their relationship to other groups of organisms. Dotted lines indicate tentative phylogenetic relationships.

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We now understand that fungi in the traditional sense are not a single systematic group but include true fungi (Fungi) as well as several small groups of fungus-like organisms. The smaller groups include the slime molds (Amoebozoa, Plasmodiophorales, Acrasiales), aquatic molds, agents of downy mildews, and agents of white rusts (all Oomycota). Slime molds are related to different groups of amoebae (protozoa), while the Oomycota belong to the Straminipila, which also include the diatoms (Bacillariophyceae) and brown algae (Phaeophyceae).

For the classification of fungi, the following endings or suffixes are used. ●● ●● ●● ●● ●● ●●

on or in living organisms, apparently without affecting them.

Fungi grow as hyphae that excrete enzymes for the digestion of organic substances they subsequently absorb through their cell wall. Fungi are dispersed in various ways, including by wind, water, and animals and through human activities. Only a few are mobile by means of flagella.

Fungi are very important in all natural ecosystems because: ●●

“-mycota” for divisions (phyla) “-mycotina” for subdivisions (subphyla) “-mycetes” for classes “-mycetidae” for subclasses “-ales” for orders “-aceae” for families

Species names are composed of two terms written in italics, e.g., Cookeina speciosa. The first word (Cookeina) is the name of the genus and is capitalized, and the second word (speciosa) is the specific epithet and is not capitalized. The two words together are the name of the species. In cases in which we are sure only about the genus, we refer to the organism as Cookeina sp. (Lat. species, abbreviated sp.).

Ecology: Fungi are heterotrophic organisms that gain nutrition by absorption from dead organic material (saprotrophic life style) or from living organisms, like plants, animals, bacteria, or other fungi. Some fungi are parasites (pathogens) that cause harm to their hosts, while other fungi live in mutualistic symbiosis with other organisms, sharing a mutual benefit. Commensal fungi live

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they are the most important organisms for the degradation of organic material (leaves, wood, etc.), contributing to the recycling process, especially in carbon and nitrogen cycles (Fig. 2.2). Some species of fungi are able to decompose lignin, cellulose, and other organic compounds that cannot be degraded by any other organism. Some bacteria produce enzymes for the degradation of wood. However, they are not able to degrade the large molecules and only decompose substances predigested by fungi. they decompose carcasses of animals in water and on land. they form mycorrhizae with the roots of many plants and are indispensable for their prosperous growth. Probably more than 80% of the terrestrial plants live in mycorrhizal associations. they are pioneers colonizing sterile substrates, like rocks, soils originating from volcanic eruptions, or surfaces without organic material due to human activities. Under these extreme conditions, fungi typically grow as lichens, living in mutualistic symbiosis with algae and/ or cyanobacteria. they are parasites that reduce the abundance of dominant species of plants or animals, contributing to the maintenance of biodiversity.

FIGURE 2.2. General aspects of fungi. A, A dead leaf decomposed by the hyphae of a fungus. B, Fungal mycelium ➤ decomposing leaves and dead wood. C, Roots of trees are in intimate contact with hyphae, probably in order to absorb nutrients liberated by the degradative activities of fungi. D, Due to the lichens on the rock, organic compounds accumulate and later allow the growth of plants. E, Lichens colonize sterile soils, such as compacted volcanic ash. F–H, Different types of fungal tissues (plectenchyma). Scales = approx. 10 μm. F, Prosenchyma formed by skeletal hyphae (Polyporales). G, Prosenchyma formed by parallel hyphae. H, Pseudoparenchyma.

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they outcompete populations of other fungi, bacteria, and other microorganisms for nutrients through antagonistic relationships and thus play important roles in the balance and dynamics of natural ecosystems. they prevent and reduce soil erosion by producing hyphae that cling to soil particles and secrete gelatinous substances. they serve as a food source for insects, mites, nematodes, snails, springtails (Collembola), mammals, and other animals. they live among bacteria and protozoa in the digestive system of animals, such as termites, playing important roles in the digestion of cellulose and other molecules.

Morphology: The basic microscopic unit of organization of most fungi is the hypha (plural: hyphae), and many hyphae in or on a substrate form a mycelium. Compact hyphae form a tissue called plectenchyma (Fig. 2.2F–H), which can

be used to build fruiting bodies. As seen by light microscopy, a plectenchyma with distinguishable hyphae organized irregularly or in parallel is called prosenchyma. In other tissues, called pseudoparenchyma, hyphae are not distinguishable due to numerous septa and the lack of space between the hyphal cells. This tissue can look like a parenchyma of a plant. In exposed or protected positions, the hyphae of the fruiting body develop spores that are liberated and dispersed.

Other fungi, called yeasts, are simple cells multiplying mostly by budding (Fig. 2.3).

Pseudofungi related to protozoa grow as amoebae or plasmodia, which are giant cells with many nuclei and lack a definite form. The hypha is a filament composed of eukaryotic cells delimited by transverse walls called septa. In most fungi, the septum is perforated by a single, central pore, which allows the passage of nuclei and cytoplasmic organelles. Hyphal cells either contain one nucleus each (monokaryotic or uninucleate), two nuclei associated with each

FIGURE 2.3. Different types of organization of fungal cells.

Introduction to the Fungi and Fungus-Like Organisms

other (dikaryotic), or numerous nuclei in each cell (polykaryotic or multinucleate). The nuclei in a given polykaryotic cell contain the same genetic material (homokaryotic) or the nuclei are genetically different (heterokaryotic). Hyphae of species of “Zygomycota” and the fungus-like Oomycota have few or no septa, contain numerous nuclei, and are called coenocytic hyphae.

Some true fungi in basal groups (Chytridiomycota and others) and non-true fungi form zoospores, which are motile mostly due to flagella. The types of flagella are important characteristics by which different fungal and fungus-like groups can be recognized. We use the following terms to distinguish different types of spores (Fig. 2.3). ●●

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opisthokont—a zoospore with one posterior flagellum acrokont—a zoospore with one anterior flagellum isokont—a zoospore with two flagella of similar structure

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anisokont—a zoospore with two flagella of similar structure but of different lengths heterokont—a zoospore with two different flagella pleurokont—a zoospore with lateral insertion of one or several flagella on the cell akont—a spore without flagella. This is the case of most true fungi.

Hyphae grow vegetatively without changing the nuclear phase, producing more hyphae, asexual spores called conidia, yeast cells, or chlamydospores with thick cell walls (Fig. 2.4).

The functions of conidia and sexual spores (see below) are multiplication, dispersal, and especially in the case of chlamydospores, long-term survival.

Many spores are single celled, but other spores consist of several or numerous cells in different positions. In addition, spores are highly diverse in morphology, size, color, thickness of the walls, and ornamentation, i.e., structures located on the surface of the walls of the spores, like warts or

FIGURE 2.4. Different types of asexual development by a hypha.

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spines. Spores are mostly dispersed passively, by wind, animals, or water.

Life cycle: The series of changes of a fungus or any other organism during sexual and asexual development are described as a life cycle (Fig. 2.5), in which the alternation of generations and nuclear phases is included. ●●

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generation—A generation is a multicellular developmental stage (e.g., a thallus, fruiting body, or mycelium) that develops between two unicellular units of reproduction (e.g., spores or gametes). In the case of plants, the gametophyte is the generation formed by cells with haploid nuclei and the sporophyte to the generation formed by cells with diploid nuclei. As fungi are not plants, the term “-phyte” is not adequate, so preferably we refer to gametothalli and sporothalli. nuclear phase—The nuclear phase depends on the number of sets of chromosomes in the nucleus. ȣhaploid ȣ (1n)—one set of chromosomes ȣdiploid ȣ (2n)—two sets of chromosomes

A nucleus changes from its diploid to the haploid stage by meiosis. A spore that contains a haploid nucleus resulting from a meiotic division is called a meiospore. In order to reach the diploid stage, a cell with a haploid nucleus has to develop a gametangium, gamete, or another fertile cell, which fuses by plasmogamy with a compatible cell. Finally, the two nuclei fuse by karyogamy. The result is a zygote. Developments related to changes of the nuclear phase are equivalent to sexual reproduction, while growth without changes of the nuclear phase and the production of mitospores are equivalent to asexual development.

A sexual cell (gamete or gametangium) contains one or several haploid nuclei that can only continue to develop when the sexual cell fuses with another sexual cell containing one or several compatible nuclei. We distinguish three different types of gametes: ●●

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spermatozoids are small, motile gametes (with flagellum or flagella), spermatia are small, immobile gametes (without flagella), and ovules are large, immobile gametes.

FIGURE 2.5. Basic diagram of the changes of generations and the cycle of nuclear phases. The simplified morphological characteristics of Blastocladiomycota (see Chapter 7.5) are used to illustrate this life cycle. Circles with different colors represent nuclei with different types of compatibility.

Introduction to the Fungi and Fungus-Like Organisms

Small and sometimes mobile gametes are designated as male, while larger, less mobile gametes are female. Ovules develop within oogonia (female gametangia), spermatozoids develop within antheridia (male gametangia), and spermatia develop at the tip of hyphae, which can be located within spermatogonia.

During fertilization (Fig. 2.6), gametes, gametangia, or hyphae with haploid nuclei fuse by plasmogamy. If two morphologically similar gametes unite, the process is called isogamy, and if one gamete is larger (female) than the other, it is called anisogamy. In the case of oogamy, a spermatozoid fuses with an ovule. The results of these types of fertilization are zygotes, cells with diploid nuclei. If a spermatium fuses with a trichogyne, the process is called spermatization. In some fungi, gametangia fuse by gametangiogamy without liberating gametes. If one gametangium is larger than the other, the larger structure is called ascogonium, in species of Ascomycota, and oogonium, in species of Oomycota, while the smaller one is called an antheridium. In the case of somatogamy, two hyphae without any special sexual development fuse by a conjugation bridge. Normally,

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two monokaryotic hyphae fuse by somatogamy and develop a dikaryotic hypha. When two hyphae with multinucleate cells fuse, a dikaryotic hypha (heterocytic type) or a hypha with multinucleate cells (holocoenocytic type) is formed.

The descriptions presented above are valid for heterothallic species of fungi, in which gametes or nuclei from two individuals with compatible genetic material are needed for sexual reproduction. In other fungi, however, haploid nuclei with identical genetic material can fuse. These fungi are homothallic, thus they reproduce sexually without the participation of another individual. By incrossing, genes might change their position on different chromosomes, but no new genotypes are produced.

Biochemical aspects:  Fungi are highly diverse, not only in their morphology and ecology but also in the chemical compounds they synthesize.

Different carbohydrates, amino acids, proteins (enzymes), cyclic compounds, and other chemical compounds are produced by different species of fungi, so these can be useful to characterize and classify the fungi. Fungi secrete numerous enzymes, called exoenzymes, like cellulases, xylanases,

FIGURE 2.6.  Different types of fertilization. Long red arrows indicate direction of movement. Short red arrows indicate growth by which compatible cells come in contact with each other and fuse.

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pectinases, lipases, or proteases, that degrade large molecules present in the substrate. Some species produce powerful, unique enzymes such as lignin peroxidases and laccases for the degradation of wood, and they might even be able to degrade compounds synthesized by humans that do not exist in the natural environment (xenobiotics). The nutrients resulting from decay are absorbed through the fungal cell walls by diffusion. Other chemical compounds secreted by fungi help to coordinate the fusion (fertilization) between gametes, gametangia, and hyphae. Many fungi synthesize substances to infect, manipulate, kill, and interact with living plant cells. Many compounds are toxic and help to eliminate other fungi, bacteria, and other microorganisms that compete for the same source of nutrients. These bioactive compounds show antibacterial, antifungal, insecticidal, nematicidal, or protozoicidal activity when the fungi grow together with other competing organisms. The active compounds can be very useful for human beings for the control of other organisms, and “bioprospecting” has been the focus of many investigators seeking to find new biologically active chemical compounds.

Importance for Humans Fungi have positive impacts on human activities (Stamets, 2005) because they: ●●

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are useful for human nutrition by producing edible fruiting bodies or metabolites (vitamins, citric acid, gluconic acid, etc.) obtained by food technology (white biotechnology) and by participating in the production of cheeses, sauces, alcoholic drinks, and sausages. have medicinal properties, produce antibiotics (e.g., penicillin and cephalosporin), are aphrodisiacs, or synthesize other substances interesting for medicine (e.g., cyclosporin and statins). produce enzymes used in detergents, vitamins, and many other chemicals used in industry. produce dyes. are pathogens of pest insects or weeds, so they are useful for biological control. contribute to the bioremediation of contaminated soils, air, and water.

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are used as model organisms for scientific investigation, especially in genetics and cell biology. participate in the decay of organic material in compost.

On the other hand, fungi have negative impacts on human activities because they: ●●

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affect our health by being poisonous or pathogenic, by producing mycotoxins in food, or by causing allergies. live as parasites on cultivated plants (Box 1) or domesticated animals, cause postharvest losses, or grow as molds on food. grow in buildings as molds or decompose wood.

For more applied aspects, see the information at the end of every chapter.

Chapter 2 Bibliography Reference for Fungi and Fungus-Like Organisms Stamets, P. 2005. Mycelium Running. How Mushrooms Can Help Save the World. Ten Speed Press, Berkeley, CA.

Further Readings on Fungi and Fungus-Like Organisms Boddy, L., and Coleman, M. 2010. From Another Kingdom, the Amazing World of Fungi. Royal Botanic Garden Edinburgh, Edinburgh.

Carlile, M. J., Watkinson, S. C., and Gooday, G. W. 2001.

The Fungi. 2nd ed. Elsevier, Academic Press, San Diego, CA. Deacon, J. 2006. Fungal Biology. 4th ed. Blackwell Publishing, Malden, MA. Dugan, F. M. 2006. The Identification of Fungi. An Illustrated Introduction with Keys, Glossary, and Guide to Literature. American Phytopathological Society, St. Paul, MN. Esser, K. 1982. Cryptogams. Cyanobacteria, Algae, Fungi, Lichens. Cambridge University Press, Cambridge.

Esser, K., and Lemke, P. A., eds. 1994-2002. The Mycota.

A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research. Vols. I–XI. Springer, New York.

Font Quer, P. 1968. Diccionario de Botánica. Edición Revolucionaria, La Habana, Cuba.

Gams, W., Hoekstra, E. S., and Aptroot, A., eds. 1998.

CBS Course of Mycology. 4th ed. Centraalbureau voor Schimmmelcultures, The Netherlands.

Introduction to the Fungi and Fungus-Like Organisms

Box 1

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Fungal Diseases of Cultivated Plants

A plant is diseased when its normal development is affected by pathogenic organisms over a relatively long period of its life or by unfavorable environmental factors (Agrios and Beckerman, 2011).

Pathogenic organisms can be fungi, insects, mites, bacteria, viruses, viroids, mycoplasmas, or nematodes (Box 12). Probably more than 70% of the plant diseases are caused by fungi.

When fungi attack cultivated plants and affect plant vigor negatively by reducing the number of leaves, flowers, and fruits, they interfere with the interests of humans who see the results of their agricultural efforts reduced. In general, growers try to minimize the damage caused by pathogens and aim to either cure their plants or maintain plant health from the beginning. Phytopathology is the scientific study of plant diseases and their control.

Three factors are important for the development of a disease: a susceptible plant, a pathogen, and favorable environmental conditions. Humans can interfere in any aspect by trying to avoid a disease or reduce its impact.

These are the most important strategies to control diseases of cultivated plants.

Selection of resistant cultivars: The cultivation of

plants that cannot be attacked by the pathogens is the most efficient and ecological way to prevent diseases.

However, resistant plants are not always available, and fungi are often able to overcome the resistance of the plant. Additionally, when a plant is genetically altered to increase its resistance, other organisms or natural mechanisms important for the survival of the plant might be affected.

Chemical control: There are many chemical products

available for the control of pests. However, they have to be applied carefully because they can have drastic impacts on the balance of the ecosystems, the environment (pollution of soil, water, and air), and our health. It is recommended to use them only when no alternative is available, and it is important to follow exactly the instructions for use recommended by the manufacturer. Natural pesticides or chemical compounds derived from antibiotic fungal secondary metabolites, such as the strobilurins, are less toxic to humans and more easily decomposed in nature. Therefore, they are considered to be more environmentally friendly than

the pesticides based on chemical compounds that do not occur in nature (xenobiotics).

Clean seeds: Many agents of diseases are dispersed

together with the seeds of the plants. Therefore, it is very important to use seeds without spores or hyphae of fungi associated with them.

Cleanliness: It is important to remove the remains

of the cultivated plants after harvest in order to eliminate the pathogens located in these remains.

Exclusion: The pathogen must not come into contact

with the cultivated host plant. The cultivation can be protected in a sealed greenhouse or by establishing the plantation far away from the area of distribution of the pathogen. In this context, quarantine rules are very important, although over the years, it may become very difficult to keep the pathogen separated from its host.

Rotation of cultivated species: Many pathogens

survive by diaspores (spores, sclerotia, hyphae) in the soil, so they are not eliminated by harvesting and they are present when the farmer sows in the same area. By culturing different species of plants, which are not susceptible to the pathogens of the species cultivated the year before, disease incidence can be reduced.

Biological control: The aim of biological control

is to establish an organism in a population of plants that will protect against infection and will be persistent over time. This works well in the case of parasitic fungi that control invasive plants or insects. Mycoparasitic fungi can be used for the control of fungal pathogens. Some fungi can protect plants from infection by antagonism, competition for nutrients, or occupying infection sites. They can also have a positive influence on plant health by increasing their vigor. Endophytes may help a plant survive adverse conditions, such as drought, and mobilize nutrients, while other fungi may stimulate the plant’s defense reaction either locally or at a distance. Due to many factors relevant for the development of the control agent and numerous interactions between different organisms, biological control is a very complicated strategy.

However, bureaucracy and lack of concise regulatory procedures coordinated among different countries (continued on next page)

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Box 1 (continued from previous page) are perhaps the most important problems that have prevented many efficient and safe biopesticides from being launched on the markets.

Control of vectors and weeds: Insects and other

animals can be vectors that promote the dispersion of diseases. Weeds can be hosts of pathogenic fungi, which are able to infect cultivated plants. Therefore, it is important to know the plants and animals associated with the cultivated plants and to control their presence.

Other strategies: Other strategies consist of

preventing environmental conditions conducive to plant disease, e.g., plants have to be planted at adequate spacing and ventilation.

Given the multitude of agents threatening a cultivated crop and the complexity of relevant factors, the application of a single control method is not enough to ensure yields in a sustainable way.

The integrated approach to pest control and disease management is the most promising. With this strategy, different control strategies are combined and a maximum number of organism interactions and environmental factors are considered.

In native tropical vegetation, plant diseases caused by native fungi are poorly known and rarely reported in phytopathological literature. Apparently, plants and fungal pathogens are in a natural balance.

Ingold, C. T. 1984. The Biology of Fungi. 5th ed. Hutchin­ son, London.

Jeffries, Y., Jeffries, P., and Young, T. W. K. 1994. Interfungal Parasitic Relationships. CAB International, Wallingford, England.

Mueller, G. M., Bills, G. F., and Foster, M. S., eds.

2004. Biodiversity of Fungi, Inventory and Monitoring Methods. Elsevier, Academic Press, San Diego, CA.

These pathogens, however, might become a problem elsewhere, especially in monocultures of the host plant. They might also jump onto a plant species closely related to its natural host species, as in the case of Chrysoporthe cubensis, which jumped from native plants of Melastomataceae onto introduced species of Eucalyptus (see Chapter 5.3.18), and Puccinia psidii, a parasite of Psidium guajava and other native Myrtaceae, which jumped onto Eucalyptus spp. and Syzygium jambos (see Chapter 4.4.2). A crop plant introduced to a new area may even be devastated by local fungal parasites because it has no resistance against them.

Box 1 Bibliography Reference for Fungal Diseases Agrios, G. N., and Beckerman, J. 2011. Plant Pathology.

6th ed. Academic Press, San Diego, CA.

Further Readings on Fungal Diseases Evans, H. C. 1995. Fungi as biocontrol agents of weeds: A tropical perspective. Can. J. Bot. 73:S58-S64.

Farr, D. F., Bills, G. F., Chamuris, G. P., and Rossman, A. Y. 1989. Fungi on Plants and Plant Products in the United States. American Phytopathological Society, St. Paul, MN. Palm, M. 1999. Mycology and world trade: A view from the front line. Mycologia 91:1-12.

Silveira, V. D. 1995. Micologia. Ambito Cultural, Rio de Janeiro, Brazil.

Wagenitz, G. 1996. Wörterbuch der Botanik. Gustav Fischer Verlag, Jena, Germany.

Further Reading from the Internet Maddison, D. R., and Schulz, K.-S., eds. 2007. The Tree of Life Web Project. Retrieved 2014, from http://tolweb.org