Stem rust

Behavior

Like other "Puccinia" species, "P. graminis" is an obligate biotroph and has a complex life cycle featuring alternation of generations. The fungus is heteroecious, requiring two hosts to complete its life cycle – the cereal host and the alternate host. There are many species in "Berberis" and "Mahonia" that are susceptible to stem rust, but the common barberry is considered to be the most important alternate host. P. graminis" is macrocyclic".



"Puccinia graminis" can complete its life cycle either with or without barberry.

"P. g. triticis obligately biotrophic lifestyle involves the dramatic up-regulation of particular gene transcriptions, constituting its biotrophy genomic features. These genomic regions have parallels in other eukaryotic plant pathogens. These parallels - between these independently evolved and unrelated sets of genes - show a strong and broad pattern of convergent evolution around the plant pathogenic lifestyle.Due to its cyclical nature, there is no true 'start point' for this process. Here, the production of urediniospores is arbitrarily chosen as a start point.

Urediniospores are formed in structures called uredinia, which are produced by fungal mycelia on the cereal host 1–2 weeks after infection. The urediniospores are dikaryotic and are formed on individual stalks within the uredinium. They are spiny and brick-red. Urediniospores are the only type of spores in the rust fungus life cycle that are capable of infecting the host on which they are produced, and this is therefore referred to as the 'repeating stage' of the life cycle. It is the spread of urediniospores that allows infection to spread from one cereal plant to another. This phase can rapidly spread the infection over a wide area.

Towards the end of the cereal host's growing season, the mycelia produce structures called telia. Telia produce a type of spore called teliospores. These black, thick-walled spores are dikaryotic. They are the only form in which "Puccinia graminis" is able to overwinter independently of a host.

Each teliospore undergoes karyogamy and meiosis to form four haploid spores called basidiospores. This is an important source of genetic recombination in the life cycle. Basidiospores are thin-walled and colourless. They cannot infect the cereal host, but can infect the alternative host. They are usually carried to the alternative host by wind.

Once basidiospores arrive on a leaf of the alternative host, they germinate to produce a haploid mycelium that directly penetrates the epidermis and colonises the leaf. Once inside the leaf the mycelium produces specialised infection structures called pycnia. The pycnia produce two types of haploid gametes, the pycniospores and the receptive hyphae. The pycniospores are produced in a sticky honeydew that attracts insects. The insects carry pycniospores from one leaf to another. Splashing raindrops can also spread pycniospores. A pycniospore can fertilise a receptive hypha of the opposite mating type, leading to the production of a dikaryotic mycelium. This is the sexual stage of the life cycle and cross-fertilisation provides an important source of genetic recombination.

This dikaryotic mycelium then forms structures called aecia, which produce a type of dikaryotic spores called aeciospores. These have a worty appearance and are formed in chains – unlike the urediniospores that are spiny and are produced on individual stalks. The chains of aeciospores are surrounded by a bell-like enclosure of fungal cells. The aeciospores are able to germinate on the cereal host but not on the alternative host. They are carried by wind to the cereal host where they germinate and the germ tubes penetrate into the plant. The fungus grows inside the plant as a dikaryotic mycelium. Within 1–2 weeks the mycelium produces uredinia and the cycle is complete.Since the urediniospores are produced on the cereal host and can infect the cereal host, it is possible for the infection to pass from one year's crop to the next without infecting the alternate host. For example, infected volunteer wheat plants can serve as a bridge from one growing season to another. In other cases the fungus passes between winter wheat and spring wheat, meaning that it has a cereal host all year round. Since the urediniospores are wind dispersed, this can occur over large distances. Note that this cycle consists simply of vegetative propagation – urediniospores infect one wheat plant, leading to the production of more urediniospores that then infect other wheat plants.

Evolution

The fungal ancestors of stem rust have infected grasses for millions of years and wheat crops for as long as they have been grown. 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.

Stem rust has been an ongoing problem dating back to Aristotle's time. An early ancient practice by the Romans was one where they would sacrifice red animals such as foxes, dogs, and cows to Robigus, the rust god. 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. Weather records from that time have been reexamined 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. Laws banning barberry were established in 1660 in Rouen, France. This was due to the fact that European farmers noticed a correlation between barberry and stem rust epidemics in wheat. The law banned the planting of barberry near wheat fields and was the first of its kind.

The parasitic nature of stem rust was discovered in the 1700s. Two Italian scientists, Fontana and Tozzetti, first explained the stem rust fungus in wheat in 1767. Italian scientist Giuseppe Maria Giovene, in his work "Lettera al dottor Cosimo Moschettini sulla ruggine", also thoroughly studied the stem rust. Thirty years later it received its name, "Puccinia graminis", by Persoon, and in 1854 brothers Louis René and Charles Tulasne discovered the characteristic five-spore stage that is known in some stem rust species. The brothers were also able to make a connection between the red and black spores as different stages within the life cycle of the same organism, but the rest of the stages remained unknown.

Anton de Bary later conducted experiments to observe the beliefs of European farmers regarding the relationship between the rust and barberry plants, and after connecting the basidiospores of the basidia stage to barberry, he also identified that the aeciospores in the aecia stage reinfect the wheat host. 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.

Due to the useful nature of both barberry and wheat plants, they were eventually brought to North America by European colonists. Barberry was used for many things like making wine and jams from the berries to tool handles from the wood. Ultimately, as they did in Europe, the colonists began to notice a relationship between barberry and stem rust epidemics in wheat. Laws were enacted in many New England colonies, but as the farmers moved west, the problem with stem rust moved with them and began to spread to many areas, creating a devastating epidemic in 1916. 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 partly prompted by the threat it posed to food supplies during the war. 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. Later, in 1975–1980, the program was reestablished under state jurisdiction. 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. A barberry testing program was created to ensure that only those species and varieties of barberry that are immune to stem rust will be grown in the quarantine area.

In 1969 two races not detected before in Australia were found and for decades one hypothesis was an African origin, and in 2018 DNA analysis confirmed that, specifically South African.

South Africa itself has an ongoing problem with various stem rust outbreaks which requires better response, including an indigenous breeding for resistance program.