Although ergot of rye causes yield reductions, the significance of the disease is primarily related to the various toxic alkaloids present in the ergots (sclerotia). The alkaloids can cause severe health problems in both humans and animals. Before this disease was understood, the ergots were ground up along with rye grains and ingested when the flour was used for baking. In the Middle Ages, this led to a frightening disease of humans known as "holy fire" or "St. Anthony’s fire." Today, ergot poisoning is mostly a concern in animals that may be given contaminated feed or graze where wild grasses are heavily infected with ergot.

(Left) Ergot on rye. Courtesy R.A. Kilpatrick. (Right) St. Anthony. From a woodcut made in Germany about 1215 A.D. Courtesy Staatliche Graphische Sammlung München, Munich, Germany. Redrawn from the original.

Symptoms and Signs

Claviceps purpurea infects only the ovary of cereal and grass plants; no other part of the plant is infected. In the early stages of disease development, a sticky exudate (honeydew) consisting of host sap and conidia often appears (Figure 2). The infected ovary is replaced by a purplish-black sclerotium, commonly referred to as an ergot (Figure 3). "Ergot" is the French word for "spur." Long ago, people in France noted some resemblance between the sclerotia and the spurs on rooster legs. Size of the sclerotium is host plant dependent. They are generally 1 to 5 times larger than the host seed. Thus, the largest ergots (1-5 cm, 0.5-2 in) are found in large seeded plants such as cereal rye. The host range for C. purpurea is largely confined to members of the grass subfamily Pooideae, the cool-season grasses such as bentgrass, bluegrass, fescue, and ryegrass.

Figure 2

Figure 3

Pathogen Biology

Sexual reproduction

Sclerotia, or ergots, are the overwintering, or survival, stage of the fungus Claviceps purpurea (Figure 1). After exposure to cold temperatures, moisture stimulates the formation of one or more tiny, stalked stromata (Figure 4). Sexual mating, which involves karyogamy to form diploid nuclei and meiosis to return to the haploid state, stimulates the production of the sexual fruiting bodies, the perithecia, and the sexual spores, the ascospores. In the spherical head of each stroma, numerous perithecia form (Figure 5). These flask-shaped fruiting bodies are filled with asci, each of which contains 8 filiform (long and thin) ascospores. Ascospores are usually forcibly discharged into the air.

Figure 1

Figure 4

Figure 5

Asexual reproduction

As the mycelium colonizes the infected ovary of the host plant flower, conidiophores and conidia are produced on the surface of the ovary. Conidia (asexual spores), which are haploid, one-celled, and elliptical (Figure 6), are exuded in droplets of honeydew (Figure 7). Splashing raindrops and insects aid in the dispersal of the conidia.

Figure 6

Figure 7

Disease Cycle and Epidemiology

Disease Cycle

Sclerotia (ergots) may be left on the soil at the end of the season or sown with the seed when cereal or grass crops are planted. The sclerotium (or ergot) is the survival or overwintering structure of C. purpurea. A period of 4 to 8 weeks of near freezing weather is required for germination of the sclerotium. Sclerotia germinate in the spring, just prior to flowering in the cereals and grasses. Ascospores are ejected into the air and are disseminated by air currents. Only those ascopores that land on a host stigma or ovary can cause infection.

The stigma of a grass flower is large and featherlike; this feature helps trap windborne pollen. This same feature traps the airborne ascospores. Ascospores, which are the primary (initial) inoculum, germinate and infect the ovary within 24 hr.

Within five days, conidia form on the surface of the infected ovary. They are exuded in a clear-to-tan , sticky, sugary honeydew (Figure 7). Conidia are the secondary inoculum and are dispersed to other flowers by physical contact, splashing rain, and insects. The honeydew attracts insects to the wind-pollinated flowers. Insects contaminated with conidia may visit healthy flowers where new infections are initiated. Conidia from ergot-infected wild grasses, particularly in fence rows, can be the primary inoculum in cereal and grass seed production fields.

Figure 7

Over time, the infected ovary develops into a hard, dark colored sclerotium (or ergot) (Figures 1,3).

Figure 1

Figure 3

Epidemiology

Claviceps purpurea is common in temperate climates in which the cold period required for sclerotial germination is met. In warmer climates, such as the southeastern U.S., sclerotia are colonized by other fungi and do not survive well.

Rainfall or high soil moisture is required for stroma formation and ascospore production. In the cereal grains and many of the grasses, resistance to infection develops after fertilization. Thus, conditions that delay or interfere with pollination, such as cool, wet weather, can increase the period of susceptibility.

Conidia are an important means of secondary spread. Any transfer of honeydew from infected to healthy flowers can lead to infection. Secondary spread can occur through any means that moves conidia to healthy flowers, including rainsplash, insects, head to head contact, and moving equipment.

Disease Management

Cultural Practices

Because ergots (sclerotia) do not usually survive for more than one year, rotation with a non-susceptible host plant is a viable management tactic for annual crops. Deep plowing buries sclerotia, so ascospores from stromata cannot be discharged into the air. Although deep plowing buries the ergots, many cereal crops are now grown with "no-till" practices in which new crops are seeded directly into the stubble from the previous crop to reduce soil erosion. Crop rotation is even more important when deep-plowing is no longer an option.

Ergot is one of the most important diseases in grass seed production. Because many of the grass species are perennial, tillage and crop rotation are not management options. Post-harvest field burning has been practiced in the northwestern U.S. to manage ergot and other diseases and pests since the 1940s, but environmental concerns have resulted in legislative restrictions to burning.

Only ergot-free seed should be planted. If seed containing ergot is planted, it should be planted at least 5 cm (2 in) deep to prevent emergence of the stromata. Wild grasses along fence rows should be eradicated or mown or grazed to prevent flowering (Figure 8).

Figure 8

Chemical Control

Chemicals have been applied to seed or soil to inhibit production of ascospsores from sclerotia, but are not economical. Recently, sterol-inhibiting fungicides have been applied to flowers to prevent infection in grass seed production, but such treatments are not usually economical in cereal production.

Genetic Resistance

Interest in genetic resistance to ergot has increased since the 1970s with the creation of male-sterile lines of wheat and barley for hybrid seed production. Wheat and barley are self-pollinated plants, unlike rye which is cross-pollinated. Effective male-sterility systems provide the opportunity for hybrid seed production, however, male-sterile plants flower longer and remain susceptible until they are fertilized. Fungicides may be necessary to protect them from infection.

Historical Significance

Although ergot causes yield reductions, concern about the disease is primarily related to the various toxic alkaloids present in the ergots. The alkaloids can cause severe health problems in both humans and animals. In the Middle Ages, a frightening disease of humans known as "holy fire" or "St. Anthony's fire" was common but unpredictable. Its history is unclear because diagnostics were primitive and symptoms could be attributed to a number of diseases. Symptoms also varied depending on which toxins, called alkaloids, were present in the ingested ergots and at what concentration. Common symptoms included strange mental aberrations, hallucinations, a feeling of burning skin or insects crawling under the skin. Women frequently miscarried, and fertility was generally reduced during outbreaks. Some victims developed gangrene due to constriction of blood vessels in the extremities; many victims lost hands and feet. (Figure 9). Patients with ergotism were cared for in hospitals dedicated to St. Anthony until their painful and prolonged sufferings ceased (Figure 10).

Figure 9

Figure 10

People under the influence of ergot alkaloids may have convulsions, become manic, appear dazed, be unable to speak or have other forms of paralysis or tremors, and suffer from hallucinations and other distorted perceptions. These strange behaviors have been linked to ergotism during the French Revolution and witchcraft in Europe and the U.S. (Salem, MA, in particular). Peter the Great was stopped at the mouth of the Volga River in 1722 in his quest for a warm-water port at Constantinople (Istanbul) by an ergot outbreak that poisoned both his soldiers and their horses.

Ergots are so commonly associated with rye that they were included in early botanical drawings of the plant species (Figure 11). This may be one reason that it took a long time for people to make the association between St. Anthony's fire and ingestion of the ergots. The discovery of the cause of ergotism in 1670 is attributed to a French physician, Dr. Thuillier. Ergotism could then be reduced by separating the ergots from the healthy grains before milling.

Figure 11

Thousands of people have died of ergotism, and mortality rates averaged 40% in some documented epidemics in the 1800s. Even after the cause of ergotism was known, many poor people did not have alternative food sources in years when ergot was severe. Many lives have probably been saved by the adoption of the potato, which originated in South America. As the potato became a peasant staple, production of rye and its accompanying ergot disease declined in many areas.

Fascination with C. purpurea has resulted in its appearance in various fictional works. Robin Cook based his 1994 novel, Acceptable Risk, on an ergot-like fungus isolated in Salem, Massachusetts. A character in an episode of the television series, X-Files, develops strange behaviors after receiving a tattoo colored with a rye extract.

Current Significance

Ergot reduces yield because seeds or kernels are replaced by sclerotia. The disease is of greater significance because of the toxic alkaloids produced by the fungus. Modern cleaning methods remove ergots from grain before it is milled or used for animal feed, but the process is costly and may leave toxic residues. The legal limit of ergot is 0.3 per cent by weight for rye or wheat and 0.1 per cent for barley, oats, or triticale. Grain is classified as "ergoty" if it exceeds this level and is of lower value. Ergot toxins are not destroyed by baking.

Modern management practices reduce ergot infections in most cereal crops. Occasionally, animals released into fields for grazing are poisoned by ergot in wild grasses, particularly following prolonged cool, wet weather in the spring. Ergot can also be a problem where cattle producers rely on grass hay for feed during the winter. When fed to cattle, levels of ergot greater than 0.3 per cent by weight can cause them to lose ear tips and other extremities during very cold weather. Ergot remains a significant problem in grass seed production by reducing yields, creating harvesting problems because of honeydew residues, and causing restrictions on shipment of contaminated seed to other countries.

Midwives and doctors have used extracts from ergots to hasten childbirth or to induce abortions for centuries. Ergot is now deliberately cultivated in the field and laboratory for medicinal purposes. Chemists have intensively studied the more than 40 alkaloids produced by the fungus, including the infamous lysergic acid diethylamide (the hallucinogen, LSD) which was synthesized in 1938. Various compounds have been isolated and modified for medicinal uses, such as treatment of migraine headaches, post-partum bleeding, and various psychological disorders.

Additional Related Fungi

Sorghum ergot. Several Claviceps species cause ergot disease in sorghum (Figure 12). In 1995, Claviceps africana was discovered in Brazil, the first report outside Africa and Asia. It rapidly spread worldwide in most sorghum growing areas including the U.S. It has been found in the Texas high plains where 90% of the U.S. and 35% of the world sorghum hybrid seed is produced. The life cycle is similar to that of C. purpurea with the addition of a second, airborne conidial stage on the surface of the honeydew droplet, in addition to the sticky conidia, which contributes to its rapid spread. The toxicity to animals appeared minimal in previous feeding studies, but the sudden threat of the disease worldwide has led to new studies to determine if the fungus is a health threat to animals in the new areas of disease occurrence. (See additional information in the APSnet Feature Article http://admin.apsnet.org/publications/apsnetfeatures/Pages/Ergot.aspx.)

Figure 12

Endophytes in grasses. Pasture grasses with superior drought and insect tolerance and competitivenss have made grazing animals sick. Investigation revealed the presence of fungal symbionts, that were named endophytes (Figure 13). These were fungi from the same family as the ergot fungus (Clavicipitaceae).

Figure 13

Figure 14

The endophytic fungi produce alkaloids similar to those produced by the ergot fungus, resulting in animal diseases such as "fescue toxicosis" and "ryegrass staggers." Symptoms are similar to those of ergotism. Because the fungi are usually transmitted only by seed, care must be taken that endophytes are not present in seed used for forage plantings. On the other hand, endophytes are beneficial in some turfgrass species because they confer disease and drought tolerance and are used as a biological control for leaf-feeding insect pests (Figure 14).

Figure 15

One species of grass endophyte, Epichloë typhina, sometimes produces an external sexual stage that halts the development of grass seed, causing a disease called "choke" (Figure 15). "Choke" disease sometimes limits the production of endophyte-enhanced grass seed.

Selected References

Bandyopadhyay, R., D.E. Frederickson, N.W. McLaren, G.N. Odvody, and M.L. Ryley. 1998. Ergot: A new disease threat to sorghum in the Americas and Australia. Plant Dis. 82:356-367. See also APSnet Feature Article: http://admin.apsnet.org/publications/apsnetfeatures/Pages/Ergot.aspx

Bove, F.J. 1970. The Story of Ergot. S. Karger, NY.

Carefoot, G.L. and E.R. Sprott. 1967. Famine on the Wind. Rand McNally, Chicago, IL

Esser, K. and A. Düvell. 1984. Biotechnological exploitation of the ergot fungus (Claviceps purpurea). Process Biochemistry 19:142-149.

Hudler, G.W. 1998. Magical Mushrooms, Mischievous Molds. Princeton University Press, Princeton, NJ

Johnston, W.J., C.T. Golob, J.W. Sitton, and T.R. Schultz. 1996. Effect of temperature and postharvest field burning of Kentucky bluegrass on germination of sclerotia of Claviceps purpurea. Plant Dis. 80:766-768.

Kren, V. and L. Cvak (eds.) Ergot: The Genus Claviceps (Kren, V. and Cvak, L., Eds.). 1999. Harwood Academic Publishers, Amsterdam, The Netherlands.

Lorenz, K. 1979. Ergot on cereal grains. CRC Critical Reviews in Food Science and Nutrition. 11: 311-354.

Mathre, D.E. (ed.). 1997. Compendium of Barley Diseases. 2^nd ed. APS Press, St. Paul, MN

Matossian, M.K. 1989. Poisons of the Past. Yale University Press, New Haven, CT

Puranik, S.B. and D.E. Mathre. 1971. Biology and control of ergot on male sterile wheat and barley. Phytopathology 61:1075-1080.

Rehacek, Z. and P. Sajdl. 1993. Ergot Alkaloids: Chemistry, Biological Effects, Biotechnology. Elsevier Publishers, NY

Schardl, C.L. and T.D. Phillips. 1997. Protective grass endophytes: where are they from and where are they going? Plant Dis. 81:430-438.

Schultz, T.R., W.J. Johnston, C.T. Golob, and J.D. Maguire. 1993. Control of ergot in Kentucky bluegrass seed production using fungicides. Plant Dis. 77:685-687.

Tudzynski, P. and J. Scheffer, J. 2004. Claviceps purpurea: molecular aspects of a unique pathogenic lifestyle. Molecular Plant Pathology 5:377-388.

Wood, G. and J.R. Goley Smith. 1982. Epidemiology of ergot disease (Claviceps purpurea) in open-flowering male sterile cereals. Ann. Appl. Biol. 100:73-82.