16

Deuteromycota: The Imperfect Fungi

Richard E. Baird

CHAPTER 16 CONCEPTS

• Taxonomy of the Deuteromycota is based on asexual spore formation or no spores produced.

• Sexual stages are primarily the in Ascomycetes, but there are a few in the Basidiomycetes.

• Species can be parasitic or saprophytic.

• Asexual spores called conidia are nonmotile.

• Conidia are formed on conidiophores either singly or grouped in sporodochia, pycnidia, acervuli, or synemmata.

Species of the Deuteromycota, also known as the imper-fect fungi, are among the most economically destructivegroup of fungi. These fungi cause leaf, stem, root, fruit,and seed rots; blights; and other diseases. The Southerncorn leaf blight epidemic in the 1970s, which caused adamage of one billion dollars, was incited by Helminthos-porium maydis, the anamorph or the asexual form of theascomycete Cochliobolus heterostrophus. Other deutero-mycetes, such as Aspergillus flavus, produce mycotoxins(aflatoxins) in infected corn kernels. Mycotoxins wheningested by humans or animals can cause cancer of thedigestive tract or other serious illnesses or death.

The deuteromycetes were called imperfect fungi inthe early literature because they were thought not to pro-duce sexual spores like those by species of the Ascomy-cota (Chapter 13 and Chapter 15) and Basidiomycota(Chapter 19). Descriptions and classifications of thesefungi were based solely on production of conidia or onmycelial characteristics, or both. Deuteromycetes are nowknown to be the anamorphic stage of members of theAscomycota and Basidiomycota. For example, Fusariumgraminearum is the imperfect (asexual) stage of Gibber-ella zeae. The ubiquitous pathogen Rhizoctonia solani,which does not produce asexual spores, is the anamorphof the basidiomycete Thanatephorus cucumeris.

DEUTEROMYCOTA OR FUNGI IMPERFECTI

A brief history of this group may be helpful in understand-ing why a fungus may be known by two scientific names.During the 1800s, fungal identification was based strictlyon morphological characters. The object of these studieswas to identify pathogenic fungi when very little wasknown about their anamorph–teleomorph (sexual spore)

relationship. The asexual fruiting bodies were often theonly structures present on infected host tissues, and sci-entists were unaware that sexual reproductive statesexisted. Early mycologists, such as Persoon (1801), Link(1809), and Fries (1821), described genera and species ofimperfect (lacking a known sexual stage) fungi that werelater classified as Fungi Imperfecti. These studies initiatedthe description of many deuteromycetes and other fungiand are considered the starting point for fungal classifica-tion. Saccardo (1899) compiled descriptions of the knownfungi into one unified source in his Sylloge Fungorumseries. Taxonomic keys and descriptions to the genera andspecies of the Deuteromycota by using spore shape, size,presence of cross-walls (septa) in the hyphae, and fruitingbody type were provided by numerous scientists over thenext half century. Conidiospore development (ontogeny)was used as a basis to identify genera and species afterthe 1950s. Asexual spore development on conidiophoresand within fruiting bodies was considered a more naturalclassification for these fungi. Although considered a morenatural classification scheme than those previously basedon spore and conidiophore morphology, the earlier sys-tems continue to be used by plant pathologists and diseasediagnosticians because of the ease in identifying the gen-era and species. Since these early works, hundreds ofpapers and monographs were developed that include addi-tional genera and species with information on their asso-ciated sexual stages.

Many of the imperfect fungi do not readily form asexual stage in culture or on host tissue. Therefore, arti-ficial systems for identification were developed and arecurrently being used. Recognizing that the majority ofdeuteromycetous fungi with a teleomorphic stage alsohave a second name for the sexual stage may be criticalin understanding how to identify these fungi.

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LIFE HISTORY

The deuteromycetes are primarily terrestrial in distribu-tion, but can occur in salt or fresh water. They survive byderiving nutrients as saprophytes on plant debris or asparasites on living hosts. The degree of parasitism orpathogenicity varies depending on the fungus, the isolate,and host they invade. Many species of deuteromycetes arenot only parasitic on plants but also infect animal cells.

Deuteromycetes may cause damage directly by infect-ing a host or indirectly by producing toxins. Direct infec-tions by deuteromycetes to living hosts, other than plants,are termed mycoses and approximately 15 types areknown. The more common mycoses include candidiosis(Candida albicans), and superficial infections called der-matophytosis, which include athlete’s foot or dandruffcaused by several Tinea species. A common species ofdeuteromycete associated with animal, avian, and humandisease is Aspergillus, which causes aspergillosis. Infec-tions may induce lesions on the surface of the skin or maydamage internal organs such as lungs and liver. Infectionfrequently occurs when hosts are under stress, and immu-nosuppressive situations result from the poor health (e.g.,AIDS virus).

Indirect damage from some of these fungi results fromingestion of infected food (feed) or through inhalation ofparticles containing mycotoxins that are either carcino-genic or cause other health problems. Mycotoxins areproduced by fungi during the growth of the crop, or duringtransportation, processing, and storage. For example, afla-toxin levels in corn increase during drought and when highlevels of nitrogen fertilizers are applied. Different typesof mycotoxins are produced by species of Aspergillus,Fusarium, and Penicillium. One of the most importantgroups of toxins is the aflatoxins produced by Aspergillusspecies and occur primarily on crops such as corn, cottonseed, and peanuts.

Another group of mycotoxins are fumonisins that areproduced by F. verticillioides ( = moniliforme) and F.proliferatum (Gelderblom et al., 1988). Fumonisin is pri-marily associated with F. verticillioides, which can rou-tinely be cultured or identified from corn tissues (Baconand Nelson, 1994). Several forms of the toxin exist, butFB1, FB2, and FB3 are the most common and importantthat are typically associated with food and feed (Gelder-blom et al., 1988). If ingested, fumonisin can cause aneurological disorder in horses, called leukoencephomal-acia, pulmonary edema in pigs, and esophageal cancer inhumans.

TAXONOMY OF THE DEUTEROMYCETES

The size, shape, and septation pattern of conidia are usedas the primary characters for the practical and workingidentification of deuteromycetes genera and species.

Conidia are defined as asexual, nonmobile spores thatbelong to the anamorphic stage of a fungus life cycle. TheSaccardian system, which used spore type to identify thedeuteromycetes, was the first major tool employed bymycologists to identify genera (Saccardo 1899). The Sac-cardian system was incorporated into other systems thatincluded more natural classification schemes based onconidial ontogeny or development. This more advancedsystem is usually referred to as “The Hughes-Tubaki-Barron System of Classification.” The work by Barnettand Hunter (1986) includes keys and descriptions for iden-tification of genera. Finally, Hennebert and Sutton (1994)identified subtle differences in spore development on con-idiophores for identifying genera and species.

MORPHOLOGICAL STRUCTURES

Conidia (Figure 16.1) are produced on specialized hyphaecalled conidiophores. Because there are a large number ofdeuteromycete fungi, much variation can occur in theirreproductive structures. Conidia vary in shape and size andcan be one- or two-celled or multicellular, depending onthe number of septa present. Septa within the spores vary,from transverse (across) to longitudinally oblique. Shapesrange from filiform (thread-like), ovoid (egg-shaped), clav-ate (club-shaped), cylindrical (cylinder-shaped), stellate

FIGURE 16.1 Condia or asexual spores can be simple or com-plex and can be single or multicellular. (Drawing courtesy ofJoe McGowen, Mississippi State University).

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(star-like), or branched. Conidia can be ornamented withappendages and appear hyaline to colored.

Conidiophores are specialized hyphae, branched orunbranched, bearing specialized conidiogenous cells at thepoints where conidia are produced. Conidiophores mayoccur singly (separate) or in organized groups or clusters.If conidiophores are formed individually (Figure 16.2) andnot enclosed in specialized structures, then the fungi thatproduce these forms are called Hyphomycetes. Thehyphomycetes are subdivided into two groups based oncolor of hyphae and spores. The dematiaceous group hasdark hyphae and spores, whereas the moniliaceous speciespossess light or pale-colored hyphae and spores. Demati-aceous genera of deuteromycetes include plant pathogenicspecies such as Alternaria, Aspergillus, Bipolaris, andPenicillium.

An example of an economically important dematia-ceous hyphomycete is Alternaria solani, the causal organ-ism of early blight of tomato. The disease caused by A.solani is considered by many to be the most economicallydamaging to tomatoes in the U.S. The disease occurs eachyear because the pathogen overwinters in plant debris insoil as chlamydospores (thick-walled survival spores). Asthe temperature warms in the spring, the chlamydosporesgerminate within the plant debris or soil, and hyphae con-tinue to grow saprophytically, forming conidia on individ-ual conidiophores. Conidia produced during thesaprophytic stage are disseminated by wind, rain, andinsects or are transported in soil on farm machinery. Forlong-distance dissemination, infected seed is the primarysource. Under wet and warm conditions, the conidia

present on the tomato plant tissue germinate and hyphaecan either penetrate the host through stomata or directlythrough the cuticle. Infections usually occur first on themature foliage. Lesions develop and conidia are producedwithin the necrotic areas of the tomato foliage or stems.Secondary infections can occur from the local dissemina-tion of new condia formed on the host and plants canbecome completely defoliated. The fungus can developchlamydospores that remain dormant in the dead planttissues to start the cycle over for the following season.Symptoms of early blight can be observed on all above-ground tomato parts. Following germination, pre- andpostemergence damping-off of plants can occur. Becauselesions are generally first observed on mature leaves, thedisease appears to progress from the lower portion, mov-ing upward to the top of the plant. Infections increaseforming circular lesions up to 4 to 5 mm in diameter, andthe lesions become brown, with concentric rings givingthe necrotic area a target-shaped appearance. Leaves thatare infected often are observed with yellowing areas. Asmultiple lesions occur from secondary infections, theleaves turn brown and die. The entire plant can becomedefoliated and die at this stage. Controls for the diseaseinclude avoiding purchase of infected seed and soil fortransplants that harbor the fungus; crop rotation with othersolanaceous plants, such as potatoes, eggplant, and pep-pers; removal or burial of crop residue; and use ofdisease-free plants, fungicides, and resistant varieties.

DEUTEROMYCETE CONIDIOMATA

If condiophores are grouped together into organized clus-ters, then they are formed within specialized structurescalled conidiomata. The different types of conidiomatainclude acervuli, pycnidia, sporodochia, and synne-mata. Modern references assign acervuli and pycnidia tothe group Coelomycetes. Sporodochia-forming speciesare considered under the dermatiaceous or moniliaceoussubgroups of hyphomycetes. Synnemata have been placedunder the hyphomycetes in the subgroup stilbaceous fungi(Alexopoulus et al. 1996).

Conidiophores and conidiomata on hosts or in cultureare used for identification. The ability of the deutero-mycetes to form these structures in culture vs. that on ahost varies per genus and species. A structure that is rou-tinely formed on a host may not often be observed whengrown in culture media. An example is setae (sterilehyphae or hairs) that are associated with acervuli of Col-letotrichum spp. Setae (sterile-like appendages) routinelyform in the acervuli produced on living hosts, but may beabsent when growing on selective medium. As most iden-tification keys are based partially on the morphology ofthe pathogen on host tissue, proper identification mayrequire direct observation of conidiomata development onplant tissue rather than on artificial media.

FIGURE 16.2 Fungi that produce conidia borne on looselyspaced conidiophores are called Hyphomycetes (Drawing cour-tesy of Joe McGowen, Mississippi State University).

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Sporodochia are similar to acervuli except that thecluster or rosettes of conidiophores form on a layer orcushion hyphae on the host surface (Figure 16.3), whereasacervuli are imbedded in epidermal tissue or the plantcuticle. Sporodochia also appear as mat-like cottony struc-tures due to the clustering of condiophores. However, inculture, sporodochia that resemble those on host materialsare rarely observed, making species identification difficult.Examples of specific genera of fungi forming sporodochiainclude Epicoccum, Fusarium, and Strumella.

Fusarium oxysporum f. sp. vasinfectum, causal agentof Fusarium wilt of cotton, is a good example of a sporo-dochia-forming fungus. The conidia of this pathogen over-winter in plant debris or can be introduced into fields byinfected seed or in soil transported by farm equipment.The fungus forms chlamydospores in the soil or in plantdebris. Under optimum weather conditions, the conidia orchlamydospores germinate and the fungus growssaprophytically, producing conidia on conidiophorerosettes. Germinating conidia or hyphae that come in con-tact with host root tissue can invade by direct penetrationor indirectly through wounded areas on the root. Rootwounding is often increased by the root-knot nematode,Meloidogyne incognita, and the occurrence of this pesthas been directly associated with fields with increasedlevels of Fusarium wilt. Following invasion into the root,the hyphae then grow inter- and intracellularly throughthe cortex and endodermis. The fungus penetrates the vas-cular system, and conidia are rapidly produced and dis-tributed systemically into the transpiration stream of thecotton plants. The fungus physically obstructs the lumens

of the xylem tissue, preventing water movement, whicheventually results in wilting and death of the plants.Chlamydospores form in dead host tissues and overwinterin the plant residue. Control practices include use of cleanseed from uninfested fields, use of resistant varieties, andreduction of root-knot nematode levels through chemicalcontrol, rotation, or with nematode-resistant varieties.

Synnemata conidiomata form conidiophores that arefused and the conidia often form at or near the apex(Figure 16.4). Species that produce conidia in this fashionbelong to the Stilbellaceae group of deuteromycetes. Con-idiophores of the synnemata-forming species are usuallyelongate and easy to identify from cultures because oftheir upright, whisker-like appearance. Synnemata aregenerally formed in culture unlike the sporodochial-form-ing species. Common genera that form synnemata areGraphium, Arthrosporium, Isaria, and Harpographium.

Graphium ulmi, the anamorph for the causal agent ofDutch elm disease, produces synnemata during the asexual

FIGURE 16.3 Sporodochia form on the surface of the host plantcontaining clusters or groups of conidiophores. (Drawing cour-tesy of Joe McGowen, Mississippi State University.)

FIGURE 16.4 Synnemata consist of fused condiophores at thebase, forming conidia at the apex or on the sides of the structure.(Drawing courtesy of Joe McGowen, Mississippi State Univer-sity.)

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or conidial stage of the life cycle. In the spring, the patho-gen, which overwinters in plant debris, grows saprophyt-ically and forms mycelia where the synnemata are pro-duced. The spores of the pathogen can then infect healthytrees by an insect vector, and if roots of healthy plantsare grafted to an infected tree, the pathogen can be trans-mitted to the healthy tree. The conidia are primarily dis-seminated by the elm bark beetle (Scolytidae) carried ontheir body parts. As the insects feed on the tree tissues,they deposit conidia into the feeding wound sites. Thefungus germinates, becomes established, and grows intothe xylem tissue. Blockage of the vascular system occursfrom the fungus and by defense responses of the host tree.Symptoms of Dutch elm disease include yellowing andwilting on one to many branches early in the season,depending on when infection occurs. Leaves of infectedtrees turn brown and die in portions of the tree or the entiretree may be affected. If the tree survives the first yearsfollowing invasion, death will occur sometime during thesecond year of infection. If stems of the tree are sectioned,a brown discoloration is observed in the outer xylem oftwigs, branches, and sometimes roots. Also, in dead anddying trees, insect larval galleries from the elm bark beetlecan be observed under the bark of the tree trunk. Controlsfor Dutch elm disease include methods to eliminate thevector and pathogen by removing dying and dead wood(sanitation — Chapter 32). Fungicides injected into thewill stop the spread of the pathogen, but treatments mustbe repeated continuously from one year to the next.

COELOMYCETES CONIDIOMATA

Acervuli (sing. acervulus) contain a defined layer of con-idiophores and conidia formed just below the epidermalor cuticle layer of plant tissues (Figure 16.5). Conidio-phores and conidia erupt through the host epidermis orcuticle exposing the acervulus. Conidiophores withinthese structures are generally short and simple comparedto the hyphomycetes, such as Aspergillus and Penicillium.Once exposed, acervuli are usually saucer-shaped inappearance (Barnett and Hunter, 1986). In culture, fungithat typically form acervuli on host tissue can often appearto produce sporodochia. The eruption of host cuticle orepidermis, which defines an acervulus, cannot be observedin culture.

An example of an acervulus-forming pathogen is Col-letotrichum lagenarium, the causal agent of anthracnoseof cucurbits. Colletotrichum lagenarium overwinters onplant debris and in seeds obtained from infected fruits.The fungus grows saprophytically in the soil and producesconidia on dead tissue. The conidia are disseminatedlocally by rainfall and soil transported on farm equipmentand over longer distances by infested seed. When weatherconditions are suitable for infection, conidia germinate onthe host. The germ tubes (hyphae) form appressoria at the

point of contact with the host cell, quickly followed byformation of infection pegs, which allow direct entry intothe host. Hyphae then grow intracellularly, killing hostcells. As the fungus continues to grow, angular light todark brown or black lesions are formed between the leafveins. The lesions are elongate, narrow, and water-soakedin appearance and become sunken and yellowish to brown.When conditions are favorable, acervuli form on stromaltissue and conidiophores containing conidia erupt throughthe cuticle of the host. Spores are exposed to the environ-ment and disseminated. Girdling of the stems or petiolescan occur and defoliation results. Control practicesinclude the use of disease-free seed, crop rotation withresistant varieties, cultural practices that remove or buryplant debris, fungicide sprays, and use of resistant cucurbitvarieties when available.

Pycnidia (sing. pycnidium) differ from acervuli by theformation of the flask-shaped structures composed of fun-gal tissue that enclose the conidia and conidiophores (Fig-ure 16.6). Pycnidia shapes described by Alexopoulus et al.(1996) include the following: papillate, beaked, setose,uniloculate, and labyrinthiform. Conidiophores that formwithin the pycnidium can be extremely short as in Phomaor larger as in Septoria or Macrophoma. Pycnidia resem-ble perithecia, which are sexual reproductive structures ofsome species of the Ascomycota (Chapter 15). If observedmicroscopically, the spores of the ascomycetes are bornein asci and not on conidiophores. Other important consid-erations when identifying pycnidia-producing deutero-mycetes is the presence or absence of an ostiole, which islocated at the apex and where conidia are exuded in athick layer or cirrhus. Keys to the identification of deuter-omycetes often refer to imbedded pycnidia within the host

FIGURE 16.5 Acervulus embedded in host tissue containingclusters or groups of conidiophores (Drawing courtesy of JoeMcGowen, Mississippi State University.)

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material, but in pure culture, pycnidia of the same fungalspecies will occur superficially on artificial media.

Septoria glycines, the causal agent of brown spot ofsoybean, produces conidia within pycnidia. The funguscan reinfect plants within the same field during subsequentyears since the conidia or mycelium overwinter on debrisof host stem and leaf tissues. During warm and moistweather, sporulation occurs as the fungus is growingsaprophytically and the conidia are disseminated by windor rain. The spores germinate and hyphae invade by pass-ing through stomata. The pathogen grows intercellularly,killing adjacent cells. Lesions and the new conidia formthat can serve as a source for secondary infections on thesame host plants. The pathogen primarily invades foliage,causing a flecking appearance on mature leaves, but infec-tions can also occur on stems and seed. If environmentalconditions are optimum, secondary infections can occur,resulting in defoliation that generally moves from thelower leaves and progresses upward. Lesions are usuallyirregular, becoming dark brown and can be up to 4 mmin diameter. During initial development of the pathogen,lesions often coalesce to form irregular-shaped spots. Onyoung plants, leaves turn yellow and abscise, but late inthe growing season, infected foliage can be rusty brownbefore falling off. Control methods are limited to the useof resistant varieties, rotation to nonhost crops, and fun-

gicides. The latter methods are generally not consideredto be economically feasible.

Species in the Mycelia Sterilia are traditionallyincluded in the Deuteromycota as a group that does notform asexual spores. Identification of these fungi is basedon hyphal characteristics, absence or presence of sclerotia(survival structures) and number of nuclei per hyphal cell.Rhizoctonia solani and Sclerotium rolfsii have teleomor-phs that place them into the Basidiomycetes (Chapter 19).Both of these fungi are important plant pathogens thatoccur worldwide and attack agronomic, vegetable, andornamental crops. Rhizoctonia solani has many morpho-logical and pathogenicity forms called anastomosisgroups.

Rhizoctonia species, which are responsible for brownpatch of turfgrass, survive as sclerotia in plant debris inthe soil. Over a wide range of temperatures, the sclerotiagerminate and the fungus grows saprophytically until asuitable host becomes available. Once the fungus becomesestablished in the host, circular lesions develop. Leavesand sheaths lose their integrity and appear water-soaked.The damaged tissue at first has a purplish-green cast,which then becomes various shades of brown dependingon weather conditions and the type of grass. Often, dark-purplish or grayish-brown borders can be observed aroundthe infected areas. Fungicide applications are effective inpreventing or reducing severity of the brown patches. Thedisease may also be controlled by the following culturalpractices: avoiding excessive nitrogen applications thatenhance fungal growth, increasing surface and subsurfacedrainage, removing any sources of shade that reduce directsunlight and increase drying of the leaf surface, and reduc-ing thatch build-up when possible.

In summary, the deuteromycetes are a very diversegroup based on the presence of conidiophores and conidia,except for the fungi that do not produce asexually. Thereader should keep in mind that when mycologists firstcreated this artificial group, the sexual reproductive stageswere unknown. Although the teleomorphs have now beendetermined for many of the deuteromycetes, these sexualstages are often rare or almost never seen on a host or inculture. As many deuteromycetes are plant pathogens, thegroup has been maintained for identification based on theirasexual reproductive structures and cultural characteristicswhen identifying members of the Mycelia Sterilia.

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Alexopoulus, C.J., C.W. Mims, and M. Blackwell. 1996. Intro-ductory Mycology, 4th ed. John Wiley & Sons, New York,869 pp.

Bacon, C.W. and P. E. Nelson. 1994. Fumonisin production incorn by toxigenic strains of Fusarium moniliforme andFusarium proliferatum. J. Food Prot. 57: 514–521.

FIGURE 16.6 Pycnidium, a flask-shaped structure composedof fungal tissue, can be either embedded in or superficial on hosttissue. Large numbers of conidiophores and conidia formedwithin the structure. (Drawing courtesy of Joe McGowen, Mis-sissippi State University).

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Barnett, H.L. and B.B. Hunter. 1986. Illustrated genera of Imper-

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