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The barberry connection with stem rust

Wheat stem rust is one of the most devastating diseases affecting wheat. A virulent strain is currently spreading from its origins in East Africa, posing a major threat to wheat production around the world. That threat level could ramp up even higher if the pathogen’s complicated life cycle includes a phase on barberry shrubs. So a Canadian researcher and his international colleagues are trying to get a better handle on this aspect of the disease.

Wheat stem rust is caused by the fungus Puccinia graminis tritici. Under conditions that favour the disease, it can result in complete crop loss within a few weeks.

According to Tom Fetch, a research scientist with Agriculture and Agri-Food Canada (AAFC) who specializes in cereal stem rust, the full life cycle of the fungus includes one phase on wheat and a second phase on barberry, the pathogen’s alternate host. “In the phase on wheat, there’s the red spore stage, which is mainly a summer stage,” he says. This stage produces urediniospores, which are able to directly infect wheat plants. These spores reproduce asexually, producing a new generation about every seven to 14 days. They can be carried by the wind for long distances.

“Then, in the pathogen’s full life cycle, the spore changes from a red spore to a black spore, or teliospore, to overwinter on wheat stubble. After overwintering, the teliospores produce spores that can infect barberry,” Fetch says.

Called basidiospores, these spores infect the barberry leaves, usually on the upper side. There the fungus produces structures called pycnia, and sexual reproduction occurs with cross-fertilization between two different mating types of pycnia. Then the fertilized fungus grows down through the barberry leaf. On the underside of the leaf, the fungus releases aeciospores, and those spores infect wheat.

The number of new strains (or races) that the fungus produces is related to whether or not it goes through the full life cycle. “New strains of wheat stem rust can develop in two main ways: asexual mutation and sexual recombination,” Fetch says.

Because the urediniospores are clones, one generation is usually the same as the next, but mutations can occur. “In areas of the world where stem rust is an issue, the [urediniospore] numbers get so high, with trillions and trillions of spores produced, that even if the mutation rate is pretty low you will get some new strains developing that way,” he notes.

“The sexual reproduction that occurs on barberry is a more dangerous mechanism because genetic recombination commonly occurs.” So it has the potential to continually produce new strains of the pathogen.

“A particularly good illustration of this can be seen in North America after the barberry eradication programs. In the old virulence surveys [before eradication], it wasn’t uncommon to see 40 or 50 different strains of wheat stem rust in a year. Currently in North America, over the last decade we’ve had only one strain in about 95 per cent of all the isolates that we collect,” Fetch says.

“So the numbers of strains are much, much lower once you eliminate the barberry host, and that makes it a whole lot easier to breed for wheat stem rust resistance.”

Common barberry (Berberis vulgaris) was the barberry species that contributed to the wheat stem rust epidemics in the first half of the 20th century in North America. “Common barberry is a native species in central and western Asia and eastern Europe. When European settlers came to the New World, they brought barberry with them. It’s an attractive-looking shrub that has nice red leaves in the fall and produces big, bright red berries that can be used for jams, jellies and pies. The plant also has some medicinal properties. And the settlers used the stems to make brooms and so on,” Fetch says. “They didn’t realize that barberry was contributing to wheat stem rust until the late 1800s and early 1900s.”

As people became aware of a link between barberry and wheat stem rust, various jurisdictions in Canada and the U.S. began to pass laws to require removal of barberry. In the three Prairie provinces, barberry was declared a noxious weed in 1917. The U.S. brought in eradication laws in 1918, and in Canada in 1919 a
federal law prohibited barberry.

Fetch says, “Starting in about 1918, particularly in the Great Plains of the U.S. and the Prairies of Canada, they pulled out all of the common barberry plants they could find. Today in the Prairie region, it would be very difficult to find one.”

These eradication efforts not only reduced the amount of rust inoculum on the Prairies, but also allowed the development of stem rust-resistant wheat varieties because wheat breeders had fewer stem rust races to deal with. Through ongoing breeding work, including the development of wheat varieties with multiple genes for stem rust resistance, the disease is currently under control on the Prairies, with the last epidemics occurring from 1953 to 1955.

Today, the Canadian Food Inspection Agency (CFIA) regulates Berberis, Mahonia and Mahoberberis plants in the barberry family. Only stem rust-resistant varieties can be imported and sold here. Some populations of common barberry still remain in certain locations in Canada. The shrubs would have to be within at least 10 kilometres of a wheat field to be a concern because the basidiospores tend to dry out and die within a few kilometres of their release from wheat stubble.

On the lookout for new strains
One of Fetch’s responsibilities is to conduct surveys in Canada to collect samples of rust species from wheat, barley and oat crops to identify the current races, watch for new ones and test their virulence. Rust researchers in other countries are also doing this type of work.

The spread of Ug99, a very virulent race of wheat stem rust, is a reminder of just how serious this disease can be. Ug99 was first detected in Uganda in 1999, when it overcame a wheat stem rust resistance gene commonly used by breeders around the world. Since then, the pathogen has mutated several more times to overcome other important resistance genes; there are now eight known variants. Many wheat varieties in Canada and around the world are vulnerable to Ug99 and its variants. This race has spread from Uganda into most of eastern Africa, over to Yemen and Iran, and as far south as South Africa.

While Canadian wheat breeders work to develop Ug99-resistant varieties, Fetch is actively involved in watching for the spread of Ug99 into the Americas. A key way it could arrive is by wind dispersal.

“There are some wind patterns that can move the pathogen’s spores from southern Africa over to South America,” he notes. “So my concern a few years ago was to find out how likely this is, and if this is possible – and it appears to be at least possible – then it would be important to monitor for invasion of Ug99 under the natural movement of wind from across the Atlantic Ocean.”

So Fetch is collaborating with José Martinelli and Márcia Soares Chaves, research scientists in Rio Grande do Sul state in southern Brazil. They are working on various rust-related activities including establishing and monitoring sentinel plots in Brazil to determine which stem rust strains are present on wheat and to watch for Ug99. Stem rust surveys are also being conducted in Uruguay and Argentina.

Barberry surveys
Another aspect of Fetch’s research involves international collaborations to conduct barberry surveys. Along with common barberry, many other species of Berberis, Mahonia and Mahoberberis are found around the world; however, in many regions, their roles as alternate hosts for rust species are unknown.

“Part of my work is to make sure we have a worldwide scope on our research to look at where things can change. So we are trying to get a handle on where barberry is actually functioning as an alternate host because it is still a big question mark,” Fetch explains. “We’re trying to determine how important barberry is in generating new Puccinia races.”

In this work, he is collaborating with Yue Jin, a world expert on barberry infection with the U.S. Department of Agriculture (USDA) Cereal Disease Laboratory. Jin has been collecting rust-infected barberry leaves from places like China, South America, central Asia and Africa, and he and his USDA colleague Les Szabo are determining which barberry species are alternate hosts for Puccinia species that infect cereal crops. It is complicated work because there are many different species of Puccinia, some that infect wheat and/or other cereal crops, and some that infect other grasses.

Fetch, Martinelli and Chaves have been surveying barberry species in Brazil for rust infections. “Initially, we are trying to determine if there is a functional barberry sexual cycle for wheat stem rust in South America. You can imagine a worst-case scenario – if Ug99 got to South America and there is a barberry alternate host for Ug99 to undergo sexual recombination and form other strains of Ug99,” Fetch says.

In late 2013, Sergio Bordignon, a Brazilian botanist, took the three researchers into the countryside to an area with many barberry bushes. “We started scouring the hillside looking at all these bushes, searching for rust infection. In one area that was in a low spot under some shade, the bushes were loaded with rust infection on the leaves. It was really exciting because as far as we knew it hadn’t been reported [that barberry in this region is acting as an alternate host for rust pathogens],” Fetch says.

The infected barberry plants are the species Berberis laurina. The researchers collected many leaf samples and examined the infections. Fortunately, the infections were not caused by Puccinia graminis or by Puccinia striiformis, which causes stripe rust.

The USDA Cereal Disease Laboratory is now working on identifying the rust species on the leaves. As well, Berberis laurina is being tested to see if it could act as an alternate host for cereal rust pathogens.

Fetch is hoping to expand the barberry surveys to other wheat-growing countries in South America. “For instance, there are barberry species in Uruguay and Argentina, but we don’t know whether or not those species have rust infection and, if they do, whether it is wheat stem rust or some other rust.”

Fetch summarizes, “So far, Ug99 has not come over to South America and we have not found a susceptible barberry that wheat stem rust can infect and have recombination on. That is good news for us in Canada.”

So, although the potential for widespread wheat stem rust epidemics in the Americas remains, wheat breeders still have some breathing room to develop resistant varieties.

April 13, 2015  By Carolyn King

Aecial infections on the bottom of Brazilian barberry leaves. Wheat stem rust is one of the most devastating diseases affecting wheat.