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Pathogen Biology

Ustilago maydis (Syn. Ustilago zeae) is taxonomically grouped with the heterobasidiomycete fungi. The life cycle of U. maydis includes three distinct stages. Diploid teliospores are formed in galls on infected hosts and are the overwintering propagules of the fungus. They are spherical to ellipsoid, olive-brown to black in color and heavily echinulated, i.e., covered with tiny spines (Figure 13). When a teliospore germinates, it forms a septate promycelium, undergoes meiosis, and forms haploid sporidia (also called basidiospores) that usually have a single nucleus (Figure 14). The haploid sporidia are easily maintained in culture which many considered to be the saprophytic stage of the fungus. Sporidial cultures can be propagated on many different media where they display considerable variation in morphology, color, size and growth (Figure 15). The non-infectious sporidia bud in a yeast-like manner (Figure 16). Under appropriate environmental conditions, genetically compatible sporidia mate and form dikaryotic infection hyphae; cells in this third stage are pathogenic and can infect corn and teosinte.

Figure 13	Figure 14
Figure 15	Figure 16

Additional details about the biology of Ustilago maydis

Mating and infection are under genetic control of two different loci, a and b. Historically, the a locus has been called the mating type locus and the b locus has been called the pathogenicity locus. In order for U. maydis to infect, mating partners (i.e., haploid sporidia that form diakaryotic hyphae) must have different alleles at both the a and b loci (e.g., a sporidium with a1b2 alleles mates with one having a2b1 alleles). Alleles from both loci have been cloned and sequenced. The a locus has two alleles, a1 and a2, and encodes components of a pheromone response pathway which mediates formation of conjugation tubes and cell fusion. When nutrients are limiting, haploid sporidia that have unlike alleles at the a locus form slender filaments that grow towards each other following pheromone gradients. Ultimately, the filaments fuse. Multiple alleles occur at the b locus which encodes DNA-binding proteins with regulatory functions. If the dikaryon that results from filament fusion has two nuclei with unlike alleles at the b locus, a vigorous infection filament forms (Figure 17). The infection filament responds to an appropriate surface of the host by forming an appressorium that allows the fungus to penetrate the host (Figure 18). Appressoria form only on living cells that are rapidly elongating. Appressoria have not been induced in vitro. Mating and penetration occur within a 12-18 hr period on plants artificially inoculated with compatible sporidia.

Figure 17

Figure 18

In the first several days of infection, infected tissues may appear slightly chlorotic, but there are few macroscopic signs of infection. Microscopic examination reveals that in these early stages, the U. maydis dikaryon behaves as a biotroph. The hyphae grow mainly intracellularly, but both host and fungal plasma membranes remain intact. The plant cells undergo normal cytoplasmic streaming even though they are invaded by the hyphae (Figure 19). Regular haustoria are not observed, but the presence of an electron-dense matrix material in between the host and fungal walls is a likely site of nutrient transfer (Figure 20.). The exact nature of the nutrients transferred is not known, but most U. maydis strains that are amino acid auxotrophs are non-pathogenic, suggesting that a simple carbohydrate may be the primary nutrient used by the fungus.

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Figure 20

Microscopic alterations such as abnormal enlargement of parenchyma cells may be seen as early as 24 hrs after inoculation. Tumors resulting from abnormal growth of host cells begin to develop as early as a week after infection. Tumors initially result from abnormal cell division and enlargement in host tissues, and fungal hyphae are relatively rare. Host cells remain alive during early stages of tumor formation, continuing to grow and divide, but the normal development of tissues is disrupted. For example, the regular pattern of venation is lost, and parenchyma cells may become extremely large. As the tumors enlarge, hyphae begin to proliferate in between the host cells rather than growing through them (Figure 21). Karyogamy (i.e., fusion of nuclei that occurs during sexual reproduction) appears to occur in early stages of tumor enlargement, and is followed by rapid hyphal proliferation in between host cells. At this stage, the hyphal walls become swollen and gelatinous, and the protoplasts lose their cylindrical shape and become spherical. By processes that are poorly understood, the spore initials enlarge and develop the pigmented, ornamented teliospore walls, which may be seen emerging from the remnants of the gelatinized hyphae (Figure 22). The fungus completes its life cycle each time teliospores form on an infected host.

Figure 21

Figure 22

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