Epidemiology of Karnal Bunt of Wheat

Blair Goates is a plant pathologist with the United States Department of Agriculture-Agricultural Research Service located at the National Small Grains Germplasm Research Facility in Aberdeen, Idaho. For over 20 years he has been involved with many areas of research on wheat bunt pathogens including cytology, ultrastructure, histology, and disease control through the use of chemical seed treatments and host plant resistance. His current interests are focused on the evaluation of germplasm for resistance to dwarf bunt and common bunt.

General aspects of the cause and development of Karnal bunt (KB) have been understood for many years. Basically, teliospores at or very near the soil surface germinate, and eventually produce secondary sporidia that become air-borne and infect spikes locally. However, the precise details of many critical steps of disease development are still poorly understood and often are a matter of opinion or conjecture. Currently in the United States the most damaging aspect of the disease is not yield or quality losses, but results from contamination of grain or seed with teliospores of the causal organism Tilletia indica which is quarantined by numerous countries.

Any level of disease is sufficient to cause concern because extremely slight levels of contamination (even a single spore) can be problematic to the movement of seed and the marketing of grain. This means KB may be a major problem even on the fringes of environmentally suitable areas. In addition, completely healthy grain can become contaminated with spores by passing through contaminated harvesting or handling equipment.

With this presentation, via the new interactive "electronic media", I hope to stimulate interaction and discussion among scientists and others which may lead to experiments designed to elucidate the fine details of Tilletia indica and Karnal bunt.

Teliospore Germination

Teliospores will germinate at temperatures of 5-25C. Germination occurs after about 12 days incubation at the optimal temperatures of 15-20C. Trace amounts of germination have been reported at 2C and 30C. Teliospores appear to be quite tolerable to relatively broad shifts in temperature and moisture while going through the process of germination. The process stops when soil becomes dry but resumes when moist conditions return. Teliospore germination per se may not be a particularly limiting factor of disease development because conditions conducive to germination can occur in many wheat growing areas when the plant canopy shades soil, and particularly under irrigation.

Teliospores go through a period of dormancy after formation in kernels. Germination is best after a period of several months of storage. It is assumed this dormancy also occurs under field conditions indicating that spores produced the previous season may come out of dormancy just prior to the time plants are heading and are susceptible to infection. Even under the best of conditions, teliospores that are beyond the period of post-harvest dormancy often germinate poorly. Tests rarely exceed 40% germination indicating additional dormancy factors. Teliospores that remain in sori do not germinate, probably because of high concentrations of inhibitors.

The few spore longevity tests that have been conducted under field conditions indicate spores do not survive more than four years. However, the tests have been conducted in only a limited number of environments. It has been suggested that extended periods of sub-freezing temperatures are detrimental to teliospore viability. However, there are indications that extended cold can induce a period of dormancy as has been described for other bunt pathogens. This induced dormancy may account for the lack of germination.

Infection

After teliospores germinate, haploid secondary sporidia are produced and forcibly discharged into the air. The sporidia can land on plants and may germinate to produce hyphae which produce additional secondary sporidia, or can reproduce additional secondary sporidia directly by budding. It has been suggested that hyphal colonies develop within the plant canopy. In addition, increase of secondary sporidia from colonies on the soil surface has been suggested. This increase in air-borne sporidia appears to be the primary factor in KB epidemiology. Secondary sporidia are produced only during periods of high humidity; the higher the better. Also, this is likely the reason that extended periods of high humidity are essential to the development of damaging levels of KB, and the reason that rainfall during heading enhances the disease. These are conditions that promote levels of disease that can be detected by normal routine examinations of grain for infected kernels. However, it seems possible that under the right circumstances during unfavorable conditions, microclimates on plant or soil surfaces might be sufficient to allow the increase of enough inoculum to produce the few infected spikes per acre that can be detected with the seed wash assay technique.

The number of teliospores in soil that are required to cause enough KB to be detectable by normal examination is unknown. Similar to above, the threshold of teliospore inoculum will likely be much less when the presence of disease is assayed with more sophisticated techniques.

Hyphae originating from the secondary sporidia are the infecting agents. The hyphae penetrate the stomatal opening of the glumes, lemmaes, and paleas and then grow intercellularly to the subovarian tissue. Hyphae then grow through the funiculus and enter the pericarp of the ovary where they increase dramatically and eventually form teliospores. Teliosporogenesus can occur 13 days after inoculation and possibly earlier.

Spikes become susceptible to natural infection as soon as the boot opens and they are exposed to air. At some point, probably within 3 weeks or less, the kernels become too mature to allow the disease (sporulation) to occur. Kernel maturity also shuts off sporulation leaving the kernels only partially diseased. Under proper environmental conditions, florets that are infected as soon as they emerge from the boot have the potential to become fully infected. Those that are infected toward the end of the susceptible period, will show only partial infection even under the best of environmental conditions. The development of the disease as it relates to kernel maturity and environmental conditions after infection is not well defined.

Nuclear Cycle

Meiosis and several post-meiotic nuclear divisions occur in teliospores prior to germination. The haploid nuclei migrate into filiform primary sporidia which produce allantoid secondary sporidia or hyphae which produce allantoid secondary sporidia. Hyphae are dikaryotic just prior to teliosporogenesus. It appears that fusion of hyphae from opposite mating types, which initiates the pathogenic dikaryotic condition, occurs sometime inside the plant because observations of apparent hyphal fusions prior to host penetration are very rare. In the other wheat bunts, caused by T. controversa, T. foetida, and T, tritici, the dikaryotic condition is formed prior to host penetration.