The Rusts and Smuts

Introduction

The rusts and smuts are perhaps the most economically important fungal plant pathogens. The rusts and smuts may be recognized by the bright orange pustules and the black powdery appearance of the host plant, respectively.

Left Image: Stem rust (Puccinia graminis) on wheat stem and leaves. Right Image: Bermuda grass smut (Ustilago cynodotis) on flowers.

The observation of plant diseases have probably been observed by mankind since the time of hunter gatherer society (Agrios, 2005). However, such observations cannot be ascertain due to lack of documentation. Although during historical time the observation of plant pathogens is certain, there is still controversy as to what plant diseases are being referred to. Cereals are considered to be the first cultivated crops (Simpson and Conner-Ogorzaly, 1986) and the earliest records of plant diseases referred to, in The Bible, are thought by some to be the rusts and smuts (Agrios, 2005; Carefoot and Sprott, 1967; Hudler, 1998; Large, 1940 ). An example that has been cited is of the first famine, as told in the Bible (Genesis 41: 25-30). Hudler (1998) names three species of rusts, Puccinia graminis, P. recondita and P. striiformis as the cause of the famine.  In this story, Joseph has interpreted the dream of Pharaoh to mean that God has revealed to him that there would be seven good years where the wheat crops would flourish, followed by seven years in which the wheat would be "blighted" causing famine. However, there appears to be more evidence that would question the conclusive identification of rust and smut as causes of diseases in the Bible. The reference to diseases such as Blast, Blight, Mildew and Brand, in the Bible and even in later historical times, have been used interchangeably, referable to other diseases (Fischer and Holton, 1957; Littlefield, 1981) or possibly not a disease at all (Littlefield, 1981). An example of the latter is the hot sirocco wind off the Arabian desert may have been the cause of "blasting" rather than rust, and even as recently as the 19th. Century, the term "mildews" was applied to rust diseases in Great Britain. 

While ancient Greeks and Romans may not have had names for rust and smut diseases, there seems to be little doubt that these diseases were observed. Aristotle, Theophrastus and Roman writers such as Vergil, Pliny and Ovid gave enough details in their writings that there is little doubt that they were referring to these groups of fungi (Littlefield, 1981; Fischer and Holton, 1957). Carefoot and Sprott (1967), specifically described how famine came about during the declining years of the Roman Empire that could, in part, be attributed to rust. The higher incidence of wheat rust was said to be due to the increase in rainfall during the three centuries following the birth of Christ (Littlefield, 1981) Ovid also described an entire ceremony for rust that also began during this period. It was believed that the origin of rust began as a punishment for mankind for the burning of a red fox caught in a chicken yard. The reenactment of this story became an annual ritual on April 19 as a sacrifice for averting rusts disease. The ritual later became an annual, sacred festival, the Robigalia, on April 25, with elaborate ceremonies and sacrifices made to the rust god, either Robigus, a male diety, or his female counter part Robigo. Sacrifices to Robigus or Robigo were made frequently made during the famine. Kavaler (1965) tells a similar story as that of Carefoot and Sprott (1967), but instead of rust being the lone pathogen, she tells of smuts, as well as other fungi that were not named. The latter occurring would seem to be within the realm of possibility given the increase rainfall during this period of time.

Today, we will discuss these two groups of diseases and the impact they have had on western cultures. We will begin with the rusts fungi since they have had the most impact, historically and economically, and continue to have significant impact. The species that we will discuss is Puccinia graminis, one of three species that cause Wheat Rust, which is probably the earliest recorded pathogen. We will also discuss Hemileia vastatrix, the cause of Coffee Rusts, a pathogen that changed the drinking habit of England and gave rise to an English stereotype and discuss the smuts in a more general matter.

The Rust Fungi

Before describing some of the impact that this group of diseases has had and continues to have on the world, let us look into the uniqueness of the life history of this fungus. Unlike most parasitic fungi, or fungi in general, the rusts do not have only one spore or two spore stages (one sexual and the other asexual), and a single host, they may have as many as five spore stages and may have two hosts. The species that we will be using as an example of a grain rust, Puccinia graminis (Wheat Rusts),  is such a rust. The spore stages for this species is as follows: 

The urediospores and teliospores are borne on wheat while the spermogonium and aeciospores are borne on what is referred to as the alternate host, barberry. The basidiospores are not borne on either hosts, and is the transitional stage that initially infects the barberry host. During the early spring, the aeciospores will infect the wheat plant. Infection of the wheat occurs in both the stem and leaves. Entry into the host occurs when the spores germinates and enters the plant through openings called stomata. Stomata are pores on the surface of the herbaceous parts of plants that allow for gas exchange to occur. However, these openings also provide an avenue for pathogens such as the rust fungi to enter. Once entry into the wheat plant has been accomplished, mycelium will grow and begin to absorb nutrient from the plant. The mycelium in the host plant will give rise to clusters of urediospores, with each cluster being produced in a uredium. As the urediospores develop, they will burst the epidermis, exposing the characteristic, rusty-colored urediospores on the surface of the plant. This stage is a "repeater stage" and is the most damaging stage to the wheat. The urediospore can infect other wheat plants throughout the spring and early summer. During late summer, just before fall, the uredium gradually converts into the telium and begin to produce the two-celled, thick-walled teliospores. The conversion is readily observed as the rusty-brown uredium becomes black as the teliospores are borne.

Left Image: Rusty pustules of uredia on leaf from: http://www.ars.usda.gov/images/docs/9918_10112/stripe_rust.jpg.  Right Image: Urediospores as seen through microscope from http://www.inra.fr/hyp3/images/6034277.jpg
Left Image: Black pustules of telia on stem. Right Image: Teliospores as seen through microscope. From http://www.apsnet.org/edcenter/intropp/lessons/fungi/Basidiomycetes/Pages/StemRust.aspx

The teliospore stage, with its thick wall is the over wintering stage and will remain dormant for the winter. The following spring, each cell is capable of germinating to produce basidia and basidiospores. What happens next is unique among the fungi. Instead of infecting the wheat plant, again, the basidiospores, instead, must infect the alternate host, the barberry and produces spermogonia on the upper surface of the barberry leaves. Each spermogonium consists of what is interpreted as female (receptive hyphae) and male (spermatia). These structures may be thought of as "eggs" and "sperms", respectively. Thus, this is the site where the "sexual act" takes place. In order to get the spermatia and receptive hyphae to "meet", the spermogonium exude a sweet, nectar that attract flies. As a fly goes from spermogonium to spermogonium, drinking the sweet liquid, spermatia become attached to the fly and becomes deposited on the receptive hyphae and begins to go through its sexual cycle. Unless this event takes place, the aeciospores, the next spore stage, will not form.  The aeciospore is the stage that will then reinfect the Wheat plant and the cycle then starts again.

Left Image: Teliospore germinating to produce basidium from http://www.apsnet.org/edcenter/intropp/lessons/fungi/Basidiomycetes/Article Images/StemRust14.jpg, (J.F. Hennen). Middle Image:  Spermogonium on upper surface of Barberry leaf and Right Image: Spermogonium section with receptive hyphae and spermatia from http://www.biology.ed.ac.uk/research/groups/jdeacon/FungalBiology/fig14_23d.jpg 
Left Image: Aecium on lower surface of Barberry leaf and Right Image: Aecium section with aeciospores from http://www.biology.ed.ac.uk/research/groups/jdeacon/FungalBiology/fig14_23d.jpg

A summary of the sequences of events in the life cycle may be viewed below:

Given the complexity of the life cycle of wheat rust, it would be safe to assume that the complete life cycle of this pathogen was not known when it was first observed during. Also, since the urediospore stage of wheat rust was the most recognizable stage of the life cycle, it will be seen that it would be the only known stage for centuries.

Following the Fall of the Roman Empire, the growing of wheat expanded to Northern Europe where it was free of wheat rust until the 8th-9th Century when the barberry was also introduced and established as more travel between Europe and Middle East, where wheat rust is thought to have first became established with wheat as an agricultural plant. Over time, farmers began to realize that there was an association between barberry and wheat rust. However, it would be several centuries before this knowledge would be acted upon

Barberry and Wheat Rust: An Answer to Eradication of Wheat Rusts?

At some point in time farmers observed that wheat rust was often worst when there were barberry bushes were nearby. By 1600, in France, the first law was enacted to control wheat rust by eliminating the barberry, even though there was not any tangible evidence connecting the two (Littlefield, 1981; Schumann, 1991). This was followed later by other European countries and this practice was also followed as America was being colonized. While this practice was maintained the Europeans settled in the New World also did bring barberry plants with them since its wood was used a source of tool handles and yellow dyes, and its fruits for jellies and sauces (Schumann, 1991). However, even if they did not, Wheat Rust would still be a problem since there are two native species of Barberry, in North America.

Despite this discovery, it would be a long and difficult path to discover the five spore stages in the life cycle of the wheat and would require literally the efforts of thousands of researchers, starting in the 18th Century before this great mystery would become unraveled.

Microscopic examination of the rust pustules, in 1767, by the Italian naturalist, Felice Fontana, revealed to him that the pustule was composed of what he called "small parasitical plants". He also noted that the pustule was actually composed of two kinds of "bodies". One was the rusty orange color that was expected and the other was black. Fontana concluded that this represented two species of fungi that were named by Persoon as Uredo linearis and Puccinia graminis, respectively.  Because the two "species" always were together, even in the same pustule, eventually led to the hypothesis that the two spores were derived from the same fungus. Anton de Bary would later observe that this hypothesis was correct in his observation that the uredia stage would eventually become the telia stage. It was finally the Tulasne brothers who turned their attention to the rust fungi in 1845 and concluded that there were five and only five spore stages and that different numbers of these spore stages could be found in different species of rust fungi. But what was the connection between the wheat host and the barberry?

In de Bary's germination experiments, he was able to germinate the urediospore stage on the host plant and the teliospore stage germinated to give rise to the basidiospore stage. However, he was unable to reinfect the wheat with the basidiospore stage. Why not? After numerous attempts to reinfect the wheat, de Bary believed, though he thought it was rather far fetched, that perhaps another plant was required. Even though there was a history of the wheat plant with barberry in this disease, the connection was not made immediately. However, it was made, and soon after discovered that it was the aeciospores of aecia stage that reinfects the wheat host. With that de Bary had solved all but but the function of spermogonium, which would remain a mystery until 1927 when when a Canadian plant pathologist, John Craigie, determined the function of this part of the life cycle.

The discovery that Barberry is the alternate host for Wheat Rust was a rather important discovery in trying to control the disease. Why? If we remove the Barberry plant, the teliospores may be produced and survive the winter, but the basidiospores will not have an alternate host to infect. The urediospore cannot survive a harsh winter and will also die. Thus, the Wheat Rust disease is ended. There was a program that was developed, in the United States, in 1918, and continued for decades, to eradicate the Barberry. This program was started to destroy Wheat Rust, but also was used as a means of employing large number of people during the Great Depression, in the 1930s. How important is the Barberry? In 1920, in the  Mississippi Valley, a circular area of 10 miles of Wheat was virtually destroyed. Agriculturalist searching the area found a single bush of Barberry, which was responsible for the damage!

Programs to eradicate the barberry were also carried out in some European Countries where they were very successful, and although, the program in the United States may have been very important in providing employment to a lot of people, it unfortunately, did not rid us of Wheat Rust which is still with us, today. Why did barberry eradication fail to rid North America of Wheat Rust but yet was successful in European countries? The problem was that the wheat growing areas in some of the Gulf States and Mexico had winters that were not as harsh as on the northern plains. Because of the relatively, mild winters, the winter wheat grown in Mexico and the Southern States allowed urediospores to over winter and would be ready to disperse in the wind, northward, up into the Canadian Wheat fields. The winter wheat, it is believed, is infected locally from "volunteer" weed wheat plants that became infected during the summer. Thus, the Barberry stage is not necessary for the Wheat Rust disease to continue in North America. While eradication of barberry did not rid the country of Wheat Rust, it did remove a significant source of infection and reduced the genetic variation of the rust since it diminished the stage where sexual reproduction would be occurring.  

Urediospore overwintering in  Mexico and gulf states dispersing northward as far as Canada.

Breeding Resistant Varieties of Wheat

It was not until varieties of Wheat, resistant to Wheat Rust, were bred that this disease was placed under some measure of control, but even this was not easily accomplished. There were a number of resistant Wheat varieties bred. This was necessary because it was realized that there were a number of different "physiological races" of Wheat Rust. Even in 1918, when the Barberry eradication program started, it was known that there were 28 different races of Wheat Rust. Each race of rust could be rendered harmless by a particular Wheat variety that was developed, but each Wheat variety was not resistant to all or even several of these 28 races. So a large number of Wheat varieties had to be developed for this reason. This was the most effective means of controlling Wheat Rusts. Unfortunately, with each new variety of resistant wheat that is developed, there were, in some instances, already physiological races of Rust that could infect this new variety, or the new variety would be resistant for several years, but then a new physiological race develops that would be able to infect the new variety. However, in a few cases, for reasons that are still not understood, genes would remain effective for many years.  One example of such a gene is the Sr31 that has been use for 30 years, is derived from the Rye grain. In addition to the Sr31 gene, that gave Wheat resistance to Wheat Rust, the chromosome segment that it was on also gave a higher yield in grain and resistance to other species of Rusts. Wheat varieties with the Sr31 segment immediately became popular world wide and by the mid 1990's losses due to Wheat Rust decline to insignificant levels. However, a new physiological race of Wheat Rust has now been discovered that has overcome resistance in Wheat varieties with Sr31.

Puccinia graminis race Ug99

A new race of Puccinia graminis was discovered in Uganda in 1999 (Pretorius, 2000) and has since been found in Kenya in 2001 and Ethiopia in 2003, and has spread from Eastern Africa across Arabian Peninsula, to Yemen in 2007 and Sudan. There is presently concern that it will spread to other wheat growing area of North Africa, the Middle East, Pakistan, India, Southeast Asia and beyond, causing major crop losses. Wheat in other continents are also at great risk since most varieties of wheat are susceptible to this new race of P. graminis as well. It is estimated that Ug99 can potentially wipe out more than 80% of the world's wheat crop, causing economic losses of up to several billion dollars and causing famine in many parts of the world. Again, we come across the problem of monoculture that has led us to this predicament. Research is now being undertaken to develop a new resistant variety to replace current ones in Africa and surrounding areas needed in order to prevent further losses from this race.

Map showing dispersal pattern and projected pattern of UG99 race of Puccinia graminis.

Coffee Rust of Ceylon (Sri Lanka)

At the same time that Europe was plagued by a number of plant diseases, between 1845-1885, another species of rust, was attacking the coffee-trees in Ceylon (presently Sri Lanka). The Coffee Rust fungus was first recorded by the Reverend Miles Berkeley, who was sent a collection from the Royal Botanical Gardens at Peradenija. Berkeley's collection of fungi from Sri Lanka was already quite large, containing 1100 collections, and this collection was different from all of them. Berkeley believed this to be a new species and named it Hemileia vastatrix and published it in November 1869.

Hemileia vastatrix was first found on coffee, in 1875, in the Madulsima district where it was associated with premature leaf drop. Even at this time it was already of concern since it had affected three acres of coffee plants. When Berkeley learned of this disease and the fear associated with it, he thought these fears to be well grounded since he had already seen what the Late Blight had done to potatoes. In his publication concerning this species, Berkeley even suggested immediate application of sulfur because this disease would be difficult to combat once it had been allowed to spread. The reason for this was because so much of the disease was within the leaf tissue that it would be difficult to combat. Unfortunately, no one paid attention to the fears of some of the growers and Berkeley. That was in 1869. In five years the coffee-leaf disease had spread over the whole island and no plantation was free of the disease.

The symptoms of the disease were subtle. The disease would initially cause premature leaf drop, during the first season, but the following season, the trees grew new leaves and all appeared normal. Pictures of the symptoms of this disease may be viewed here. However, leaf drops became more and more frequent and in the next five years, coffee production dropped by more than 50%. However, action by the government was slow. A commission was set up to study the disease. By this time the disease had spread to southern India and Malaysia and was menacing the entire coffee industry in the East. Two studies were done. The earlier one was undertaken by Daniel Morris.

Morris was not trained in mycology and had little understanding of fungi. However, he did know of Berkeley's suggestion that sulfur should be tried. Following application of sulfur he noted that the superficial fungal growth that could be observed on the coffee plant was eliminated and that the diseased plants looked better. However, this effect was temporary and the disease soon returned. Repeated application might have eliminated the disease when it was first observed in a small area, but with the Monsoon winds blowing the spores throughout all of the plantations, spraying a few infected plants would have little effect on this fungus. Also, Morris had misinterpreted the symptoms that were observed on the diseased plants. These and other questions would be answered by Morris's successor, Harry Marshall Ward.

Ward, unlike Morris, was trained in plant pathological methods and was a student of Anton de Bary. Upon his arrival in Sri Lanka, he could not help but be impressed with the array of fungi and other organisms that were present in. Ward isolated spores from fungi that were found the coffee plant. He found no less than 51 different fungal spores on the coffee plant which he was able to germinate and grow on a sugar gelatin substrate. One fungus included the external growth that Morris had observed to be covering the coffee plant, but Ward was able to demonstrate that this was not the fungus that was responsible for disease of coffee. Ward also observed that the actual coffee rust was largely an internal parasite that grew through the stomata of the leaves. Ward would also discover the other stages of spores that grew from the coffee rusts, but did not discover all of the spore stages, which today still are unknown, i.e. the alternate host is still unknown. Knowledge of such a host would offer an opportunity to break the life cycle of this disease and perhaps end this disease or at least diminish the losses suffered from this disease.

Although Ward would go on to discover the presumed origin of the coffee rust, and the reason for the "sudden" spread, he learned early that little could actually be done about the disease itself. When the plantation owners carved out their estate, they cut down many of the tall trees that would have sheltered them from the Monsoon winds and the rust spores that were disseminated as well. This displeased the plantation owners since they wanted Ward to discover a method by which they would be rid of the disease.

In its natural environment, the rust, was not a significant pathogen since it was an obligate parasite on the coffee plants and the coffee plant were sparsely distributed (true of most plant pathogens). However, as the land was cleared, and other species eliminated in favor of the coffee plants, this provided the ideal situation for an epidemic of the coffee rusts. Because now, there was continuous acres of coffee plants and what discontinuity was present, was short, which was not too far for the wind to carry to the next plantation. There was not even mixed cultivation which would have broken the rusts cycle since it would not have been able to attack another crop. Like Morris, Ward also suggested spraying sulfur, but at a specific time during the life cycle of the fungus, i.e. during the germination of the urediospore, when the fungus was most vulnerable. Once inside the host, the spray would be almost useless since it would not penetrate the leaves of the plant. This solution did slow the rate of destruction and raised the yield of coffee for a short time, but Ward realized this would not stop the rusts since by this time it was too late because of the vast number of infected trees with the astronomical numbers of spores that were produced from them, the disease could not be stopped.

A stereotype of British Culture also developed as a result of Coffee Rust. Prior to the Coffee Rust, coffee was an important part of the social and political environment in England. By 1675 there were approximately 3000 coffee houses, in London, which became gathering places for social, political as well as religious discussions. It was a place where the daily papers, desks and writing material were available. Lloyds of London, an international insurance company started in a coffee house, in 1690. So many ideas were discussed in coffee houses that King Charles II labeled coffee houses "seminaries of sedition" and tried to have them all closed. However, the popularity of coffee was such that when news of his edict was learned, there was so much protest that Charles was forced to rescind his order. However, when when the Coffee Rust eventually destroyed the coffee plants in Sri Lanka, Java, Sumatra and eventually spread to Arabia, Liberia and Africa. The British, no longer able to grow coffee, simply gave it up, and began growing tea instead. Thus, this is why Indian tea now is the main stimulant consumed by the British, and the drink that we now associate with England, but this was not always the case.  

Today coffee is grown mostly in the new world tropics, i.e. Columbia, Brazil, etc., and for over 100 years they were successful in excluding the coffee rusts. However, these countries now are also confronting the coffee rust. In 1970 the coffee rust was inadvertently introduced into Brazil and has now taken its toll on coffee. An intensive spraying program has controlled the disease somewhat, but with the political unrest that occurs in that part of the world, quarantine has largely been unsuccessful. Some newer means of controlling the coffee rust has emerged since Marshall Ward, but none which can be regarded as successful. Breeding programs have produced rust-resistant cultivars of coffee and other natural species exist, which are also resistant, have been cultivated, but neither have been desirable since the coffee produced is of a poor quality. The loss of desirable qualities in a crop is a common result of breeding resistance to diseases.

The realization that the disease could have been treated so easily brought about the concept of "preventive" treatment of plant diseases that are largely internal. As was the case in other crops that we have discussed, genetic uniformity was again one of the reasons that led to the destruction of the coffee crop. In the case of the Coffee rust, even crop rotation, changing to a different crop at different times of the year could have broken the rust life cycle.

Other Rusts

White Pine Blister Rust

Some rust diseases occur on trees. One of the most economically important species is Cronartium ribicola, the cause of White Pine Blister Rust disease. As was the case in Wheat Rust, there are five spore stages and an alternate hosts.  It was introduced into the United States in 1900 with White Pine seedlings from Germany. It soon rapidly spread throughout the natural distribution of White Pine forests and caused such great economic losses that it, along with the Chestnut Blight and Dutch Elm Disease prompted legislation to protect U.S. borders from entry of possibly diseased organisms. This was what led to the 1912 Federal Quarantine Act. As in the case of the Wheat Rust, the alternate host, Ribes, the genus that includes gooseberries and currants,  was not an economically important plant, was selected for eradication to control the disease. This method of control proved successful in most and some eradication programs continue to this day. Only in the Western United States was it not successful. However, breeding of resistant cultivars of White Pine began in 1952 and became available for replanting forests in 1972. Also, in some countries the fruits of gooseberry and currant plants were considered more valuable than White Pines and breeding resistant varieties of Ribes were developed there instead of resistant pines.  As you might expect by this time, new physiological races of rusts have now been discovered that are capable of infecting these varieties have been reported.

Left Image: Aeciospore stage of White Pine Blister Rust and Right Image: Information poster for eradication of Ribes, alternate host from http://www.apsnet.org/edcenter/intropp/lessons/fungi/Basidiomycetes/Pages/WhitePine.aspx

Some Rusts Occurring in Hawai‘i

There are a number of rusts that occur in Hawai‘i. Too many to cover in any detail. Instead, some selected species of interest will be summarized.

Among fungi, demonstrating that there are species that are endemic or native to a given area is difficult to demonstrate. However, among obligate parasite, host selection is often very restrictive and can be used as a criterion for demonstrating if a fungus is endemic or native.

Left Image: Atelocauda digitata on Acacia koa phyllodes and Right Image: Endoraecium hawaiiense also on Acacia koa. These two species are thought to be species of rusts that are endemic to Hawai‘i. Images from Dr. Don Gardner.

 There are also a number of introduced species that are of some economic significance. Two examples are given below.

Left Image: Coleosporium plumeriae, Plumeria Rust, introduced from Florida. Right Image: Puccinia psidii, Guava Rust, introduced from Brazil. Image from Marli F. S. Papa.Capable of infecting many species from Myrtle Family. Concern is raised of presence in Hawai‘i since there are a number of native species in this family.

Smut, The "Dirty" Fungus

The literal meaning of smut is "dirt or excrement". However, it has come to mean something that is "filthy or obscene". Like the rust fungi, the smut fungi is also a member of the division Basidiomycota, do not produce fruiting bodies and produce basidia and basidiospores from germination of the teliospore. However, unlike the rusts, the plant pathologists war against the smuts have been a successful one. Although no mention is specifically made of this group of disease until 1700, most plant pathologists agree that with the number of spores that are produced by the fungus and the number of species that grow on crop plants that smut must surely have been known since the onset of agriculture.

Mathieu Tillet, a keeper of the mint, in France, was a man of many interests. One of these included studying the problems of farmers. In 1755, while observing the smuts on Wheat, Tillet discovered that there were two types of smut growing on Wheat: La carie or what the English called "Common Bunt" or "Stinking Smut". Grains infected with this type of smut seemed healthy, at first glance, but grains were actually filled with brownish balls full of a black, foul-smelling powder (Figure 1). In the second type of smut, the plants looked healthy enough, but were covered with a loose, black powder that readily blew away. Tillet called this le charbon or what the English called "loose smut" (Figure 2). The distinction between the two types of smut was verified a century later, in 1847, by Louis and Charles Tulasne. To honor Tillet, they named the "Stinking Smut" Tilletia caries

Fig. 1:Seeds infected with Tilletia tritici (Stinking Smut), on left, and healthy seeds, on right. Courtesy J. Riesselman, copyright-free. Fig. 2: Bermuda Grass infected with Ustilago cynodontis, an example of a loose smut. Note powdery appearance of plant covered with spores.

So Tillet was delighted when, in 1750, the Academy of Arts and Sciences at Bordeaux announced that a prize would be given for the best investigation into the smutting of Wheat. Through conversations with farmers and experiments on a small parcel of land that he owned, Tillet observed that when smutted Wheat seeds were planted, the Wheat plants that grew always were smutted regardless of when he planted, whether they were planted in manure or not or the weather conditions in which they were planted. From this observation, Tillet concluded that the smut was seed borne and that the black powdery spores were the cause of the disease. In addition, he experimented with washing the seed grains, in water, cattle urine and lye solutions. Although this did not prevent the smut from forming, the treatments did suppress the disease to some degree. For his work, Tillet was awarded for the best research concerning the smutting of Wheat. However, the science in his research was actually not that conclusive. Tillet's concept of washing the seeds before planting did lead other researchers to continue in this line of investigation. The most important being Prévost, who continued with washing seeds, fifty years later.

Prévost placed smut spores in water and observed them through his microscope, over a period of several days, and saw "stubby sprouts" growing from the black particles, i.e., germination of the teliospores. He guessed from this observation that the "pointed ends" of sprout somehow pushed their way into the soft tissue of the germinating Wheat seedling and destroyed the grain. However, Prévost never saw the mycelium growing into the plant, but in his observation of germinating spores did, accidentally, discover a means of destroying the infection on the seeds.

When Prévost germinated the smut spores in water that he had distilled, he observed that they did not germinate as readily as when he used well water, and when they did germinate, the "sprout" grew for several hours and then shriveled and died. Prévost believed that when he distilled the well water, an element essential to the growth of the spores must have been removed. Although this experiment successfully killed the fungus in his lab, it would be impractical for the farmer since they would not be able to distill the water when they watered their Wheat nor could he distill rain water. Because this line of experimentation proved impractical, Prévost was ready to abandon it when he happened to hear a boastful farmer's remark that there was no smutted Wheat on his farm and that there had not been any for years. By this time, many farmers had followed Tillet's practice of washing the seeds with various solutions, before planting. However, as was the case with Tillet, this did not stop smut from forming. What was this boastful farmer doing that others were not? Prévost's conversation with the farmer did not seem as though it was going to lead to a remedy to the smutted Wheat. Then the chance statement by the farmer led to the revelation. The farmer mentioned that he washed his seeds in a copper caldron while his neighbors used wooden vats. Returning to his lab, Prévost examined the still that was used to make the distill water in which the spores did not sprout. It, too, was made of copper. With further experiments, Prévost determined that the slightest amount of copper prevented germination of the smut spores.

In 1807, Prévost recommended soaking seeds in a copper sulfate solution before planting. Although farmers were slow to adopt his suggestion, the practice was widely used from about 1850 until 1900, when  formaldehyde replaced copper sulfate. Formaldehyde was preferred since copper sulfate was found to injure or kill the embryo of the seed if carelessly used. Later mercury compounds were used and most recently hexachlorobenzene (=HCB). This method, known as topical chemotherapy, has been successfully used and has saved billions of tons of food material by killing the disease causing organisms before they can infect the plant. However, this method could not be successfully utilized in Loose Smut of Wheat.

The loose smut is not found on the surfaces of seeds, but instead infect the seed as it develops. Thus, the fungus is protected by the seed, itself. Chemicals that were initially  applied to eliminate the fungus from the embryo usually destroyed the embryo of the seeds as well. For a long time a method discovered by Jensen, a Danish plant pathologist, in 1888, was used for controlling this disease. Wheat seeds were soaked in hot water. The soaking induced hormones to form in the embryo that protected it from the fungus. However, systemic fungicides have been developed that can successfully eliminate the fungus without harming the seed. To date, there has not been any known resistance, by the smut fungi, to the fungicides that have been developed.

A Story of the Origin of Gingerbread

Although it was cited it Carefoot and Sprott (1967) and Large (1940) I was unable to find any other verifications about the following story that I am about to tell, but thought it was interesting enough to tell, anyway. Once Wheat has been contaminated with Stinking Smut, there is nothing to do but to dispose of the grain. However, there is an interesting story concerning the origin of the gingerbread that is related to Stinking Smut. It seemed that a baker ground the contaminated grains into flour and attempted to make bread with it. However, because of the horrendous odor of that the bread had when made with contaminated flour, the black discoloration in the bread and the awful taste, he was unable to sell the bread. However, he did not want to waste the contaminated grain, but what was he to do? He experimented with ways in which he could disguise all of the distasteful characteristic of the flour until he came up with a recipe that his customers would find acceptable. He used molasses to cover the dark coloration of the flour, but what could hide the taste and odor? He finally came upon a spice that was both strong in taste and odor, ginger. Thus, the origin of gingerbread. An interesting story, but one that I was unable to verify, other than in the two sources I cited.

Mycological Terms

Aeciospore: One of five spore stages in some rusts fungi, e.g., Puccinia graminis. Spore stage produced on lower surface of Barberry leaves. Spore stage must infect Wheat Plant and cannot reinfect Barberry.  

Alternate Host: Said of rust species that require two host to complete their life cycles, e.g. Wheat Rust has Barberry as its alternate host. The other host is Wheat.

Barberry: Alternate host of Wheat Rust.

Basidiospore: Spore characteristic of division Basidiomycota. In rusts, one of five spores stages, e.g., Puccinia graminis. Stage borne from germination of teliospore and must infect Barberry, the alternate host.

Basidium: Structure on which basidiospores are borne, characteristic of division Basidiomycota.

Blasting: Biblical reference to diseases of plants.

Coffee Rust: An economically important species of rust, which ended commercial coffee growing in the Old World Tropics. Most Coffee is now commercially grown in the New World Tropics, where until 1970, the Coffee Rust was excluded.

Loose Smut: Smut diseases in which the plants looked healthy, but plants were covered with a loose, black powder that readily were blown away and dispersed by wind.

Mildew: As used in this lecture, another biblical reference to diseases of plants.

Receptive hyphae: Element of spermogonium, in rust fungi. May be thought of as female portion of life cycle. Spermatia carried to receptive hyphae, by flies, in Wheat Rust. The mixing of the two different nuclei provides the continual genetic variation in the rusts that has made them difficult to with breeding of resistant varieties of Wheat.

Robigalia: A religious ceremony practiced for over 1700 years, which involved sacrificing reddish colored animals, such as dogs or cows to the Rust Gods, so that they would spare their grain crops. The origin of this ritual lay in the belief that humans were punished with rust-infected crops following an incident in which a 12 year old boy caught a fox in his father's chicken coop, and sadistically tied a bit of straw to the fox's tail and set it on fire before releasing it. As punishment, the god Robigus destroyed the wheat crop with an illness that left the plants with reddish-brown lesions as if burned by fire.

Robigo and Robigus: The Roman Godess and God of Rust. The Romans believed them to be the cause of Wheat Rust.

Rusts: Common name of economically important pathogenic fungi, belonging to the division Basidiomycota. Common name given because of the “rusty” appearance caused by disease, in urediospore stage. Many species parasitic on grain crops. Characterized by lack of fruiting bodies, formation of basidia and basidiospores from germination of teliospores and having as many as five spore stages and two hosts, e.g., Puccinia graminis (=Wheat Rust)

Smuts: Common name of economically important pathogenic fungi, belonging to the division Basidiomycota. Common name given because of the black, powdery appearance of infected host plants, in teliospore stage. Many species parasitic on grain crops. Similar in characteristic with rusts, but having fewer spore stages.

Spermatia: Element of spermogonium, in rust fungi. May be thought of as male portion of life cycle. Spore-like structures that is carried to receptive hyphae, by flies, in Wheat Rust. The mixing of the two different nuclei provides the continual genetic variation in the rusts that has made them difficult to with breeding of resistant varieties of Wheat.

Teliospore: One of five spore stages in some rusts fungi, e.g., Puccinia graminis. In Wheat Rust, a two-celled, thick-walled, spore that over winters and germinates to give rise to basidia and basidiospores.

Urediospore: One of five spore stages in some rusts fungi, e.g., Puccinia graminis. Repeating stage of rust fungi. Can continually reinfect a host as long as conditions are favorable for growth of fungus. Spore stage causing most damage in host plant.

Wheat Rust: A rust pathogen of wheat that is of world wide significance. Probably one of the oldest diseases known since wheat has been cultivated since the beginning of western civilization.


Most of this lecture was based on the following books. If you are interested in reading a more detailed account of the above stories, you may find them in Hamilton Library.

Agrios, G.N. 2005. Plant Pathology. Burlington, MA : Elsevier Academic Press

Carefoot, G.L. and E.R. Sprott. 1969. Famine on the Wind. Angus & Robertson Ltd., London.

Fisher, G.W. and C.S. Holton. 1957. Biology and Control of the Smut Fungi. Ronald Press Company, New York.

Hudler, G.W. 1998. Magical Mushrooms and Mischievous Molds. Princeton University Press, New Jersey.

Kavaler, L. 1965. Mushrooms, Molds, and Miracles. The John Day Company, New York.

Large, E.C.  1940. Advance of the Fungi. Henry Holt & Company, New York.

Littlefield, L.J. 1981. Biology of the Plant Rust: An Introduction. Iowa State University Press, Ames.

Simpson, B.B. and M. Conner-Ogorzaly. 1986. Economic Botany: Plants in Our World. McGraw-Hill, New York.


Questions to Think About

  1. The rust fungi are somewhat unique, relative to other fungi. What were some of the unique characteristics that can be observed in this group of fungi?
  2. Why was the eradication of the Barberry successful in controlling Wheat Rust in Europe, but not in North America?
  3. What is another method that has been tried in North America in order to minimize the losses due to Wheat Rust?
  4. In the story of Joseph, "rust" was never specifically used to describe the Wheat Rust. What was it called in the Bible? Do you think that the pathogen causing the famine was actually Wheat Rust? (there is no right or wrong answer here)
  5. Wheat Rust had always been a problem during the Roman Empire, why did the rust problem become so much greater just before the fall of the Roman Empire that famines were occurring?
  6. The Coffee Rust fungus had always been around. Yet in a matter of a few years, it destroyed all of the cultivated coffee in Ceylon (=Sri Lanka). Why was there all of a sudden this coffee rust epidemic? This question applies to just about all plant pathogens!
  7. In controlling seed borne smut, Prévost believed that washing the seeds in distilled water somehow prevent smut from attacking the seed. However, he was wrong. What was the actual reason that prevented smut from infecting seeds? 

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