Stem rust

Model of a spore of puccinia graminis, late 19th century, Botanical Museum Greifswald

There is considerable genetic diversity within the species P. graminis, and several special forms, forma specialis, which vary in host range have been identified.

• Puccinia graminis f. sp. avenae, oat
• Puccinia graminis f. sp. dactylis
• Puccinia graminis f. sp. hordei, barley
• Puccinia graminis f. sp. lolii
• Puccinia graminis f. sp. poae
• Puccinia graminis f. sp. secalis, rye, barley
• Puccinia graminis f. sp. tritici, wheat, barley[8][9][10]

P. graminis 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.

There are multiple pathotypes (including QCC and MCC) affecting barley, within forma specialis tritici.[9][8][10]

The stem rust fungus attacks the parts of the plant that are above ground. Spores that land on green wheat plants form a pustule that invades the outer layers of the stalk.[5] Infected plants produce fewer tillers and set fewer seed, and in cases of severe infection the plant may die. Infection can reduce what is an apparently healthy crop about three weeks before harvest into a black tangle of broken stems and shriveled grains by harvest.[1]

Stem rust of cereals causes yield losses in several ways:[11]

• Fungus absorbs nutrients that would otherwise be used for grain development.[11]
• Pustules break through epidermis, which disrupt the plant's control of transpiration and can lead to desiccation and infection by other fungi.[11]
• Interference with plant vascular tissue leads to shriveled grains.[11]
• The fungus weakens the stems, which can lead to lodging (falling over). In severe cases lodging can make mechanical harvesting impossible.[11]

Life cycle of Puccinia graminis

Like other Puccinia species, P. graminis is an obligate biotroph (it colonizes living plant cells) 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.[11] There are many species in Berberis and Mahonia (and their hybrid genus x Mahoberberis) that are susceptible to stem rust, but the common barberry is considered to be the most important alternate host.[1] P. graminis is macrocyclic[11] (exhibits all five of the spore types that are known for rust fungi[12]).

Animated video of the life cycle of stem rust

Puccinia graminis can complete its life cycle either with or without barberry (the alternate host).[11]

Puccinia graminis produces all five of the spore types that are known for rust fungi.[11]

Spores are typically deposited close to the source, but long-distance dispersal is also well documented.[1] The following three categories of long-distance dispersal are known to occur:[1]

• Extremely long-distance dispersal

This can occur unassisted (the robust nature of the spores allows them to be carried long distances in the air and then deposited by rain-scrubbing) or assisted (typically on human clothing or infected plant material that is transported between regions).[1] This type of dispersal is rare and is very difficult to predict.[1]

• Step-wise range expansion

This is probably the most common mode of long-distance dispersal and usually occurs within a country or region.[1]

• Extinction and recolonisation

This occurs in areas that have unsuitable conditions for year-round survival of Puccinia graminis – typically temperate regions where hosts are absent during either the winter or summer.[1] Spores overwinter or oversummer in another region and then recolonise when conditions are favorable.[1]

A number of stem rust resistance genes (Sr genes) have been identified in wheat.[13] Some of them arose in bread wheat (e.g. Sr5 and Sr6), while others have been bred in from other wheat species (e.g. Sr21 from T. monococcum) or from other members of the tribe Triticeae (e.g. Sr31 from rye and Sr44 from Thinopyrum intermedium).

None of the Sr genes provide resistance to all races of stem rust. For instance many of them are ineffective against the Ug99 lineage.[13] Notably Ug99 has virulence against Sr31, which was effective against all previous stem rust races. Recently, a new stem rust resistance gene Sr59 from Secale cereale was introgressed into wheat, which provides an additional asset for wheat improvement to mitigate yield losses caused by stem rust. Singh et al. (2011) provide a list of known Sr genes and their effectiveness against Ug99.[13]

There is considerable variation among Sr22 alleles, with some conferring resistance and some susceptibility.[14]

There has been significant uptake of resistant wheat varieties among Ethiopian farmers since 2014[15][16] - a great deal of which is thanks to CGIAR and CIMMYT (the International Maize and Wheat Improvement Center).[17][16]

Sr14 does not protect seedlings against TTKSK[18] but does provide moderate resistance at later stages.[18] It is effective against TTKST.[18]

Although Sr5, Sr21, Sr9e, Sr7b, Sr11, Sr6, Sr8a, Sr9g, Sr9b, Sr30, Sr17, Sr9a, Sr9d, Sr10, SrTmp, Sr38, and SrMcN are no longer effective in Lebanon, Sr11, Sr24, and Sr31 still are which is diagnostic for the presence of various races of stem rust - but the complete absence of Ug99 specifically - from Lebanon.[19]

The fungal ancestors of stem rust have infected grasses for millions of years and wheat crops for as long as they have been grown.[5] 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.[5]

While Ug99 wasn't discovered until 1999, stem rust has been an ongoing problem dating back to Aristotle's time (384-322 B.C).[11] An early ancient practice by the Romans was one where they would sacrifice red animals such as foxes, dogs, and cows to Robigus (fem. Robigo), 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.[11] 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.[11] 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.[11] The law banned the planting of barberry near wheat fields and was the first of its kind.[11]

Later, the parasitic nature of stem rust was discovered in the 1700s.[11] Two Italian scientists, Fontana and Tozzetti, first explained the stem rust fungus in wheat in 1767.[11] Italian scientist Giuseppe Maria Giovene (1753–1837), in his work Lettera al dottor Cosimo Moschettini sulla ruggine, also thoroughly studied the stem rust.[20] 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.[11] The brothers were also able to make a connection between the red (urediniospore) and black (teliospore) spores as different stages within the life cycle of the same organism, but the rest of the stages remained unknown.[11]

Anton de Bary later conducted experiments to observe the beliefs of 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.[11] 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.[11]

Due to the useful nature of both barberry and wheat plants, they were eventually brought to North America by European colonists.[11] Barberry was used for many things like making wine and jams from the berries to tool handles from the wood.[11] Ultimately, as they did in Europe, the colonists began to notice a relationship between barberry and stem rust epidemics in wheat.[11] 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.[11] 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.[11] 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.[11] Later, in 1975–1980, the program was reestablished under state jurisdiction.[11] 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.[11] 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.[11]

In 1969 two races not detected before in Australia were found[21] and for decades one hypothesis was an African origin,[21][22] and in 2018 DNA analysis confirmed that,[22] specifically South African.[21]

South Africa itself has an ongoing problem with various stem rust outbreaks which requires better response, including an indigenous breeding for resistance program.[22]

• Chilean wheat cycle
• List of Puccinia species

• Borlaug Global Rust Initiative
• FAO
• Animation of stem rust life cycle
• "Norwich Rust Group". Norwich Rust Group. Retrieved 2020-12-18.

• Bhardwaj, S.C.; Nyar, S.K.; Prashar, M.; Kumar, J; Menon, M.K.; Singh, S.B. (1990). A pathotype of Puccinia graminis f. sp. tritici on Sr24 in India. Cereal Rusts and Powdery Mildews Bulletin. pp. 35–38.