| Puccinia graminis | |
|---|---|
| Scientific classification | |
| Kingdom: | Fungi |
| Phylum: | Basidiomycota |
| Class: | Pucciniomycetes |
| Subclass: | Incertae sedis |
| Order: | Pucciniales |
| Family: | Pucciniaceae |
| Genus: | Puccinia |
| Species: | P. graminis |
| Binomial name | |
| Puccinia graminis Pers., (1794) |
|
| Synonyms | |
|
Dicaeoma anthistiriae |
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The stem, black or cereal rusts are caused by the fungus Puccinia graminis and are a significant disease affecting cereal crops. An epidemic of stem rust on wheat caused by race Ug99 is currently spreading across Africa, Asia and most recently into Middle East and is causing major concern due to the large numbers of people dependent on wheat for sustenance. The strain was named after the country where it was identified (Uganda) and the year of its discovery (1999).[1] It spread to Kenya, then Ethiopia, Sudan and Yemen, and is becoming more virulent as it spreads.[1] Scientists are working on breeding strains of wheat that are resistant to UG99. However, wheat is grown in a broad range of environments. This means that breeding programs would have extensive work remaining to get resistance into regionally adapted germplasms even after resistance is identified.[1]
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There is considerable genetic diversity within the species P. graminis and several special forms, forma specialis, which vary in host range have been identified.
Like other Puccinia species, P. graminis has a complex life cycle featuring alternation of generations, the fungus is also heteroecious which means that its various life cycle stages require alternate host species. The complete life cycle of P. graminis requires barberry as well as a cereal species.
In the spring and summer, stem rust infections on cereal plants produce dikaryotic urediniospores, which are spread by the wind to nearby cereal plants, where they germinate and infect cereals by penetrating through the stomata. This polycyclic asexual phase can rapidly spread the infection over a wide area. Towards the end of the growing season, the rust converts to producing teliospores, which again contain these two haploid nuclei of opposite mating types. Before the winter, the nucleii fuse to form a diploid cell, which remains dormant until the next spring when it undergoes meiosis to produce four haploid cells known as basidiospores, borne on a structure called a basidium. The basidiospores then undergo a mitotic nuclear division to produce the mature basidiospore which contains two haploid nuclei of the same mating type. Basidiospores cannot infect cereal plants, but are instead, carried in the wind, and infect young leaves of common barberry (Berberis vulgaris) or other susceptible Berberis, Mahonia, or Mahoberberis species or cultivars. On barberry, the basidiospore penetrates the leaf epidermis directly, and the resulting infections produce specialized infection structures called pycnia (or spermagonia).
Pycnia (or spermagonia), which result from infection on young barberry leaves by basidiospores, are the sexual stage of the fungus life cycle. When a receptive hypha from one pycnium has been fertilized by pycniospores (or spermatia) from a mating type compatible pycnium, its haploid cells become dikaryotic. The fertilized hypha forms an aecium, on the underside of the barberry leaf, which produces chains of aeciospores surrounded by a bell-like enclosure of fungal cells. Like the urediniospores and like the cells of the aecium, each aeciospore contains two nuclei. Aeciospores are carried by the wind, and infect cereals by penetrating through stomata. After infecting a cereal plant, the aecispores develop and form uredia under the plants epidermis, these produce the dikaryotic urediniospores. These uredia eventually rupture the plant's epidermis and again spread by the wind to nearby cereal plants, continuing the lifecycle.
The stem rust fungus attacks the parts of the plant which are above ground. Spores that land on green wheat plants form a pustule that invades the outer layers of the stalk.[1] The site of infection is a visible symptom of the disease. Where infection has occurred on the stem or leaf, elliptical blisters or pustules called uredia develop. Infected plants produce fewer tillers and set fewer seed, and in cases of severe infection the plant may die.
Pycnia typically form on the upper side of barberry leaves, and aecia form within 5–7 days after fertilization on the lower side of the leaf directly below each fertilized pycnium.
Left: thin section through a Chara antheridium, note the layer of non-reproductive cells around the inner reproductive cells; right: spermatozoids in long strings of spermatozoid-producing cells from an antheridium.
Ug99, which has the designation of TTKS, is a race of black stem rust (Puccinia graminis tritici).[2]
It was discovered in Uganda, Africa in 1999 and has since spread to many other African countries.[3] It is a race of black stem rust TTKS caused by the fungus Puccinia graminis tritici and is historically the most devastating fungal disease to wheat and barley that can result in 100% crop loss.[4] This strain of wheat rust, located in Ugandan wheat fields, received its abbreviated name based on the country and year in which it was found.[4] Seven races belonging to the Ug99 lineage are now known and have spread to various wheat-growing countries in the eastern African highlands, as well as Zimbabwe, South Africa, Sudan, Yemen, and Iran.[5] While it is devastating South Africa and Middle Eastern wheat production and is expected to make its way into Pakistan and the Indian subcontinent, it has yet to enter the United States.[6] This exclusive variety of wheat rust is devastating to the production of the crop because it kills 80-90% of global wheat cultivars under suitable conditions, according to the Food and Agricultural Organization of the United Nations.[4] Worldwide, this strain of wheat stem rust is a threat to global wheat production threatening food securities in developing countries.[4]
It is virulent to the great majority of wheat varieties.[7] Unlike other rusts, which only partially affect crop yields, UG99 can bring 100% crop loss. Up to 80% yield losses were recently recorded in Kenya. [8] The blight was first noted in Uganda in 1999 and has spread throughout the highlands of East Africa. In January 2007, spores blew across to Yemen, and north into Sudan. In March 2007, FAO announced its concern regarding the spread through Iran based on Iranian authorities report.[9]
Unlike other variations and species of wheat rust, Ug99 and its variants differ from other strains of the Black Stem Rust (BSR) pathogen due to their ability to overcome resistance genes in wheat that have been durable against the BSR pathogen for decades.[10] These resistant Sr genes, of which 50 are known, confer different resistance to stem rust.[11] The virulence in Uganda was associated with Sr31 and is specific to Ug99.[11] The massive losses of wheat that have occurred have been devastating, but in recent years the wheat rust epidemic has been effectively controlled through selection and breeding for these Sr genes.[11] The United States Department of Agriculture (USDA) researchers are testing genes to substantiate their Ug99 resistance, which will ultimately aid in developments of wheat varieties that will be able to fight off the rust.[6] USDA researchers have stated that resistance has been identified in spring wheat land races and that they are now studying winter wheat land races where resistance is more probable.[6] Due to the fact that the screening of the winter races is more challenges, results from the studies are not expected for another five to seven years.[6] In addition to the research being conducted by the USDA, The United Kingdom’s Department for International Development (DFID), along with The Bill & Melinda Gates Foundation, announced in February 2011 that they will by granting $40 million dollars to a global project led by Cornell University to combat deadly strains of Ug99.[12] The five-year grant to the Durable Rust Resistance in Wheat (DRRW) project will support attempts to identify new resistance genes as well as reproduce and distribute rust resistant wheat seeds to farmers.[12]
Ug99 is a member of the Phylum Basidiomycota within the Kingdom Fungi. The characteristic rust color on stems and leaves is typical of a general stem rust as well as any variation of this type of fungus. Different from most fungi, the rust variations have five spore stages and alternate between two hosts. Wheat is the primary host and barberry is the alternate host. The first stage, referred to as Stage 0, begins in the Spermogonium and is the sexual reproduction stage. The Spermogonia emanates sweet nectar that attracts flies while encouraging the spermatia and receptive hyphae to “meet”. When the nectar is released and the flies come to drink the liquid the spermatia attach to the fly and are placed on the hyphae by way of the fly, thus beginning sexual reproduction. This step in the cycle is very important, and if it does not take place, the next phase will not occur. Stage 1 takes place in the aeciospores of the aecia. These spores are binucleate and are formed in a chainlike series. They are born on barberry and are spread by the wind and are the spores that actually infect the wheat. Urediniospores in the uredia are the summer spores of the following stage, Stage 2, and are the source of the characteristic rust spots that arise. Urediniospores are the most damaging spore to the wheat and can infect other plants throughout the spring and summer months due to the spores being distributed by the wind. Stage 3, referred to as the resting stage, gives rise to teliospores, also called resting spores, in the telia. This is an overwintering stage, and when spring comes around, each teliospore is capable of germination of basidia and basidiospres. The final stage, Stage 4, is the transitional stage where the reproductive basidiospores in the basidia infect the barberry host.
The fungal ancestors of stem rust have infected grasses for millions of years and wheat crops for as long as they have been grown.[1] According to Jim Peterson, professor of wheat breeding and genetics at Oregon State University, "Stem rust destroyed more than 20% of U.S. wheat crops several times between 1917 and 1935, and losses reached 9% twice in the 1950s," with the last U.S. outbreak in 1962 destroying 5.2% of the crop.[1]
While Ug99 wasn’t discovered until 1999, stem rust has been an ongoing problem dating back to Aristotle’s time (384-322 B.C).[13] An early ancient practice by the Romans was one where they would sacrifice red animals such as foxes, dogs, and cows to Robigo or Robigus, the rust god.[13] They would perform this ritual in the spring during a festival known as the Robigalia in hopes of the wheat crop being spared from the destruction caused by the rust.[13] Weather records from that time have been observed and it has been speculated that the fall of the Roman Empire was due to a string of rainy seasons in which the rust would have been more harsh, resulting in reduced wheat harvests.[13] The first laws banning barberry were established in 1660 in Rouen, France. This was due to the fact that European farmers had correlated a relationship between barberry and stem rust epidemics in wheat.[13] The law banned the planting of barberry near wheat fields and was the first of its kind before the parasitic nature of stem rust was discovered in the 1700s.[13]
Two Italian scientists Fontana and Tozzetti first explained the stem rust fungus in wheat in 1767.[13] Thirty years later it received its name, Puccinia graminis, by Persoon and in 1854 the Tulasne brothers discovered the characteristic five-spore stage that is known to some stem rust species.[13] The brothers were also able to make a connection between the red (urediniospore) and black (teliospore) spores as different stages within the same organism, but the rest of the stages remained unknown.[13]
Anton de Bary later conducted experiments to observe the beliefs of the European farmers regarding the relationship between the rust and barberry plants and after successful attempts to connect the basidiospores of the basidia stage to barberry, he also identified that the aeciospores in the aecia stage reinfect the wheat host.[13] Upon de Bary’s discovery of all five spore stages and their need for barberry as a host, John Craigie, a Canadian pathologist, identified the function of the spermogonium in 1927.[13]
Due to the useful nature of both barberry and wheat plants, they were eventually brought to the United States by European colonists.[13] Barberry was used for many things like making wine and jams from the berries to tool handles from the wood.[13] Ultimately, as they did in Europe, the colonists began to notice a relationship between barberry and stem rust epidemics in wheat.[13] Laws were enacted in many New England colonies, but as the farmers moved west, the problem with the stem rust moved with them and began to spread to many areas, creating a devastating epidemic in 1916.[13] It wasn’t until two years later in 1918 that the United States created a program to remove barberry. The program was one that was supported by state and federal entities and was prompted by the looming fear of food supplies during the war.[13] The “war against barberries” was waged and called upon the help of citizens through radio and newspaper advertisements, pamphlets, and fair booths asking for help from all in the attempt to rid the barberry bushes of their existence.[13] Later, in 1975-1980, the program was reestablishes back to state jurisdiction.[13] Once this happened, a federal quarantine was established against the sale of stem rust susceptible barberry in those states that were part of the program.[13] A barberry testing program was created to ensure that only the species of barberry and other variations of plants that are immune to stem rust will be grown in the quarantine area.[13]