Lecture 07: 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 (Fig. 1) and the black powdery appearance (Fig. 2) on or within the host plant, respectively.

The occurrence of plant diseases have probably been recognized since the time of hunter-gatherer society (Agrios, 2005). However, such observations cannot be verified due to lack of documentation. Also, plant diseases were unlikely to be a problem at this time since the density of the plants that were utilized as food were not in dense clusters as those grown as crop plants. With the start of agriculture and civilization, plant diseases then, and also now, became a problem since now crop plants were grown in dense clusters, which "invited" various plant pests seeking food to invade agricultural land. Plant diseases were then recognized and their descriptions written down. However, what plant diseases these descriptions refer to were not always clear. 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 is often cited of the first famine, is 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 was an interpreter of dreams and was tasked with determining the meaning of an ominous dream of an unnamed Pharaoh of Egypt at the time. In his dreams Pharaoh was standing by the Nile, when out of the river came seven sleek and fat cows. They were then followed by seven thin, hungry cows that ate the fat cows. He then awakened and fell asleep only to have another dream where seven heads of healthy grain arose from a single stalk, and after, seven more heads of grain sprouted that were now thin and blasted by the east wind. The thin grains swallowed the seven healthy ones and Pharoah woke again. 

Joseph's interpretation of Pharaoh's dream was that the meaning of the two dreams were the same and that it was God telling him that there would be seven good years, when the wheat crops would flourish, followed by seven years in which the wheat would be "blighted," causing famine. With this knowledge, grains were stored for the seven good years when the grains flourished in order to prepare for the years that the grains would be blighted. However, there appears to be more evidence that would question the conclusive identification of rust as the cause of the crop failure during the famine. Both Hudler (1998) and Carefoot and Sprott (1967) both interpreted the reference of the "east wind" in Pharoah's dream was responsible for cooler weather and a great deal of rain, creating an environment favorable to the growth of rusts. Recent evidence, however, Krom, et al. (2002) has demonstrated that it was a drought rather than rust disease that was responsible for crop failure. At the time of the famine, there was a shift in climatic conditions, such that the African monsoons that was normally responsible for rainfall and the flooding of the Nile, which was the means by which crops were irrigated, greatly diminished at this time, causing crop failures to occur. 

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 Virgil, 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. It 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 The 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 rust 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 deity, or his female counterpart, Robigo.  Sacrifices to Robigus or Robigo were made frequently 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 in the world today. The species of rust that occur on wheat that we will discuss is Puccinia graminis, one of three species that cause rust on this host, and is is probably the earliest recorded pathogen of wheat. We will also discuss Hemileia vastatrix, the cause of Coffee Rusts, a pathogen that changed the drinking habits of England and gave rise to an English stereotype.  Additionally, we will discuss the smuts in a more general manner.

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 rust fungi. Unlike other parasitic fungi, or fungi in general, the rusts usually do not have only one 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, as is the case in P. graminis (Black Stem Rust). The spore stages for this species are as follows:

• • Spore Stage II: Urediospores in uredia (sing.=uredium)

  • Spore Stage III: Teliospores in telia (sing.=telium)

  • Spore Stage IV: Basidiospores on basidia (sing.=basidium)

  • Spore Stage 0: Spermogonia (sing.=spermogonium) (consists of Receptive hyphae and Spermatia [sing.=spermatium])

  • Spore Stage I: Aeciospores in aecia (sing.=aecium)

The urediospores (Figs. 3 and 4) and teliospores (Figs. 5 and 6) are borne on wheat, while the spermogonium (Figs. 7, 8 and 9) and aeciospores (Figs. 10 and 11) are borne on barberry and referred to as the alternate host. The basidiospores stage is not borne on either host, and is the transitional stage that arises from the teliospore stage. The basidiospore is the stage that forms the initial infection on barberry. The aeciospore stage re-infects the wheat plant and the cycle will start over again. Infection of the wheat occurs in both the stem and leaves. Entry into the wheat plant occurs when the spores germinate and enter 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 inside the host plant and give rise to clusters of urediospores that burst through the epidermis of the plant, exposing the rusty-colored spores on the surface of the host (Fig. 3) and is the reason for the common name given to this group of pathogens. Each cluster of urediospores produced is a uredium. The urediospore stage is a "repeater stage", reproducing itself asexually, and is the most damaging stage to the wheat host. The urediospore continues to infect other wheat plants throughout the spring and early summer. During late summer, just before fall, the uredia will gradually convert into the telia and begin to produce the two-celled, thick-walled teliospores. The conversion is readily observed as the rusty-brown uredium becomes black (Fig. 5), as the teliospores are produced.

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 a basidium and four basidiospores (Fig. 7). What happens next is unique among the fungi. The basidiospores, instead of infecting the wheat plant again, now infect the alternate host, the barberry, and produces spermogonia (Fig. 8) 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 "sperm," respectively. Thus, this is the site where the "sexual act" takes place and where new genetic variations will arise. 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. The hyphae that results from the fusion of the spermatia to the receptive hyphae will grow through the lower surface of  the infected leaf and the next spore stage, the aeciospores, is formed.  The aeciospore is the stage that will then re-infect the wheat plant, and the cycle then starts again.

The entire life cycle is summarized below:

Given the complexity of the life cycle of P. graminis, it is not surprising that the complete life cycle of this pathogen was not known for a long time. For most of the history of this pathogen, only the urediospore stage was known and it was not until the 19th. Century that most of the other spore stages were discovered. 

Following the fall of the Roman Empire, the growing of wheat expanded to Northern Europe, where it was free of Black Stem Rust until the 8th-9th Centuries, when the barberry was also introduced. Over time, farmers began to realize that there was an association between the presence of barberry and the occurrence of rust on wheat. However, it would be several centuries before this knowledge would be acted upon.

Barberry and Black Stem Rust: An Answer to Eradication of Black Stem Rust?

By 1600, in France, the first law was enacted to control P. graminis by eliminating the barberry, even though there was not any tangible evidence connecting the two (Littlefield, 1981; Schumann, 1991). This practice was followed later by other European countries.  It was also enacted as America was being colonized; however, as the Europeans settled in the New World, they 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, Black Stem Rust would still have become 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.  The fact that 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 affirm 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 re-infect the wheat with the basidiospore stage. Why not? After numerous attempts to re-infect 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, deBary did eventually make the connection and later also discovered that it was the aeciospores that re-infects the wheat host. Thus, de Bary had solved all but the function of spermogonium, which would remain a mystery until 1927, 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 Black Stem 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 Black Stem 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 Black Stem 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 Black Stem Rust? In 1920, in the Mississippi Valley, a circular area of 10 miles of Wheat was virtually destroyed by Black Stem Rust. 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 Black Stem Rust which is still with us, today. Why did barberry eradication fail to rid North America of Black Stem 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 survive the winter, and they 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 Black Stem Rust disease to continue in North America. While eradication of barberry did not rid the country of Black Stem 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.  

Breeding Resistant Varieties of Wheat

It was not until varieties of wheat resistant to Black Stem 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 Black Stem Rust. Even in 1918, when the Barberry eradication program started, it was known that there were 28 different races of Black Stem 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 Black Stem Rust. Unfortunately, with each new variety of resistant wheat that was 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, then a new physiological race developed 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, which has been use for 30 years, and is derived from the rye grain. In addition to the Sr31 gene which gave wheat resistance to Black Stem 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 worldwide, and by the mid 1990's, losses due to Black Stem Rust declined to insignificant levels. However, in 1999, a new physiological race of Black Stem Rust had been discovered that has overcome resistance in wheat varieties with Sr31.

Puccinia graminis race Ug99

A new race of P. graminis was discovered in Uganda in 1999 (Pretorius, 2000).  It 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 areas of North Africa, the Middle East, Pakistan, India, Southeast Asia and beyond, causing major crop losses. Wheat in other continents is 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, i.e. lack of genetic diversity of a crop, 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 Ug99. Currently, Ug99 has not spread as rapidly as anticipated, but have expanded to 13 countries, with 13 genetic variants that have evolved (Pratt, 2017). Egypt is the most recent country where Ug99 has been detected in 2014 and present all along the east coast of Africa (Pratt, 2017). Some resistant wheat varieties have been developed and have been tested in countries where Ug99 is present. Although successful, new genetic combinations are now occurring. 

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 varieties, and this collection was different from all of them. Berkeley believed this to be a new species and named it Hemileia vastatrix and published regarding it in November, 1869.

Hemileia vastatrix was first found on coffee in 1875, in the Madulsima District of Sri Lanka, 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 that 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 of 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 issues would be resolved 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. Ward isolated spores from fungi that were found on 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. For example, 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.

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 estates, 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 plants were sparsely distributed.  However, as the land was cleared and other species were eliminated in favor of the coffee plants, this provided the ideal situation for an epidemic of the coffee rusts, because now, there were continuous acres of coffee plants.  What discontinuity was present, was short, but was not too far for the wind to carry spores 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 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 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.

Today coffee is still grown in about 80 countries and where coffee is grown the coffee rust also occurs. Hawaiʻi was about the only coffee growing region in the world where coffee rust was not present. However, in October 2020, it was found on the island of Maui and by January 2021, it has now been found on all the major islands of Hawaiʻi. See summary of the story in the local FoxNews link below:

https://www.hawaiinewsnow.com/2021/07/24/coffee-leaf-rust-spreads-across-state-hawaii-farmers-race-save-their-crops/ 

The countries and the amount of coffee exported in these countries can be found here. After the spread of the coffee rust to most of the coffee growing areas of the old world, the only place free of the pathogen was in the new world. For over 100 years, the new world coffee growers 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. There are two species of coffee that are commercially grown, Coffea arabica and C. canephora. More than 75% of the coffee grown is C. arabica because, in term of quality, it is the most desirable species. Unfortunately, it is also the most vulnerable to coffee rust. Coffea canephora does not have same desirable taste as C. arabica and is not as commonly grown for that reason. However, because it has twice the caffeine as C. arabica, there is a market for this species. Also, it is resistant to coffee rust. Breeding programs have produced approximately 40 rust-resistant cultivars of coffee, but as in the case of black stem rust, coffee rust is constantly evolving and eventually is able to infect the new coffee varieties (Arneson, 2011).  Other natural species which are also resistant have been cultivated, but none of these 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 Black Stem Rust, there are five spore stages and 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 Black Stem 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, 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 had now been discovered which were capable of infecting these varieties.

Some Rusts Occurring in Hawai‘i

There are a number of rusts that occur in Hawai‘i. There are 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. However, among obligate parasites, host selection is often very restrictive and can be used as a criterion for demonstrating if a fungus is endemic or native.

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

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 fungus is also a member of the division Basidiomycota.  It does not produce fruiting bodies and produces basidia and basidiospores from germination of the teliospore. However, unlike the rusts, the plant pathologists’ war against the smuts has been a successful one. Although no mention is specifically made of this group of diseases until 1700, most plant pathologists agree that, given 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, including studying the problems of farmers. In 1755, while observing the smuts on wheat, Tillet discovered that there were two types of smut growing on it. The first was 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 21). 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 22) 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.  

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.  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 in 1888 by Jensen, a Danish plant pathologist, 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 "Smutty" Origin of Gingerbread?

According to Carefoot and Sprott (1967)[pages 66-67], the recipe for gingerbread owes its origin to flour smutted by Tilletia caries. The following story of its origin as told by Carefoot and Sprott is given below:

One would scarcely expect to get a delightfully edible product from a plant disease as dirty and destructive as smut. But long ago, somewhere in France or England, it is not known which, a baker found himself with a few sackfuls of flour that had been milled from smutty grist. He tried to make bread from it, but the smutty flour made dirty looking loaves, and, what was worse, the dead-fish stench of bunt that came from the hot oven sent his customers away holding their noses. The baker threw his dirty threw his dirty flour aside as worthless until one day the solution of his problem came to him. If he made little cakes sweetened with treacle, the dark molasses would mask the color of the smutted flour. And if he could get rid of the rotten taste, he might be able to sell the whole mess to his unsuspecting customers. Remembering a strange condiment that had been newly shipped from Cathay, a spice that was both pungent and hot to the tongue, the baker planned a recipe, mixed the dough, and baked the little cakes. And so gingersnaps were discovered. Generations of happy little boys and girls, munching hot gingerbread, successor to the gingersnap, and reciting,

Run, run as fast as you can,

You can't catch me-

I'm the Gingerbread man,

have never suspected that this popular cake was invented solely to save a medieval baker some money during a bad smut year.

However, Dr. Alice Ross, a food professional teacher, writer, researcher and collector at her Hearth Studios, in Smithtown, New York, believes the story is unlikely to be true. The reason that she gave me was that during the Medieval Period, when spice was first used in Western Cultures, it was a very precious commodity and that a baker would have been more likely to dispose of smutted flour rather than using something as expensive as ginger for the purpose of masking the taste and odor of the contaminated flour. Spices, in general, were far too valuable a commodity to be wasted for such a purpose. Also, Dr. Ross is an expert on gingerbread and has quite a different story on the origin of ginger bread on her web page that you can read here. 

A story similar to Carefoot and Sprott's can be found in Hunter, R., et al. (1897)[page 669], Large (1940)[page 70]  and Walker (1904)[page 389]. However, their stories do not claim any origin to gingerbread, but merely suggest that molasses and ginger are added by bakers to smutted flour to mask the color, taste and odor. Also, it appears that it was a practice occurring during the times in which their books were published, e.g. late 19th Century to early 20th Century.

Literature Cited

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.

Hunter, R., Williams, J.A., Herrtage, S.J., et al. 1897. The American Encylopaedic Dictionary. R.S. Peale and J.A. Hill, Chicago and New York.

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

Krom, M.D., J.D. Stanley, R.A. Cliff and J.C. Woodward. 2002. Nile River sediment fluctuations over the past 7000 yr and their key role in sapropel development. Geology 30 (1): 71-74.

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.

Walker, J.B. 1904. The Twentieth Century Home Encyclopedia and Gazetteer. James Randolph Walker, Irvington, New York.

Important Terms and Concepts

Aeciospore: In rust, one of five spore stages, e.g., Black Stem Rust, found on Barberry, the alternate host and is the spore stage that infects the wheat plant that gives rise to the urediospore stage.

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

Barberry: Alternate host of Black Stem Rust.

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

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.

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 Goddess and God of Rust, respectively. The Romans believed them to be the cause of Black Stem 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 uredospore 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 (=Black Stem 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.

Teliospore: One of five spore stages in some rusts fungi, e.g., Puccinia graminis. The spore stage that over winters and germinates to give rise to basidia and basidiospores during the spring season.

Urediospore: One of five spore stages in some rusts fungi, e.g., Puccinia graminis. Essentially the means of asexual reproduction. Can continually reinfect a host as long as conditions are favorable for growth of fungus. Spore stage causing most damage in host plant. In areas where winters are mild, this spore stage can persists during winter month and by pass the teliospore stage.

Black Stem Rust: Common name of Puccinia graminis, 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.

Questions to Think About

1. What are some unique characteristics about rusts diseases?

2. What was the reason for the Robigalia celebration in ancient Rome?

3. What are the 5 spore stages in Puccinia graminis (Black Stem Rust) and their functions?

4. What is an alternate host in the rust life cycle. What is the alternate host of Black Stem Rust?

5. Anton de Bary was unable to discover the function of the spermogonium. What is the function and who made the discovery?

6. What methods were/are utilized in trying to control Black Stem Rust?

7. What is the U99 strain of Black Stem Rust and why is it important?

8. What has led to the problems having to do with the U99 strain of Black Stem Rust?

9. Where and when was Coffee Rust first discovered.

10. Until 2020, what was the one place that commercially cultivated coffee was Coffee Rust not known to occur?

11. How did Coffee Rust change the drinking habit of England?

12. Which rust is a significant problem for a species of Native Hawaiian plant?

13. What are the two categories of smuts and how do they differ?

14. What are some means to control smuts?

15. Why are smut diseases more easily controlled than rust diseases?

16. What is Huitlacoche?