Yellow rust crosses continents – and could threaten one of the world’s most important crops

A yellow stripe on a wheat plant may look like a local problem. But the rust fungus causing the yellow rust disease may cross continents, trigger new epidemics and leave previously resistant wheat cultivars vulnerable.

This is the finding of a global study of 3,240 yellow rust samples collected over 15 years in 41 countries across six continents. The work involved a large international network and several hundred collaborators, coordinated by Aarhus University. The researchers document 10 cases in which specific types of rust moved between continents. In seven cases, their arrival was followed by major epidemics.

The analysis also uncovers a previously underestimated route by which new strains of rust can emerge. Two strains growing in the same wheat leaf may exchange entire cell nuclei, replacing roughly half the pathogen’s genetic material in one step and creating a new combination with unpredictable consequences.

“We had a clear sense that these things were connected. When an epidemic appeared in one place, outbreaks with similar characteristics were sometimes observed later in distant regions or on other continents. What is new is that we can now track the rust strains genetically and document how they move and evolve,” says Mogens Støvring Hovmøller, Professor at the Department of Agroecology of Aarhus University, Denmark.

Wheat supplies around one fifth of the world’s calories and protein. When a single highly epidemic rust strain spreads across several continents within a few years of its first detection, the consequences extend far beyond individual fields. It can affect cultivars grown in many countries and undermine resistance that plant breeders have spent years building up.

How yellow rust becomes a global problem

Yellow rust is caused by the fungus Puccinia striiformis, which attacks wheat and other cereal crops and forms characteristic yellow stripes on the leaves. Infections can reduce grain yields, but the problem does not end with a single harvest. New strains of rust can also overcome the resistance that plant breeders have built into wheat cultivars.

“It is not just about finding rust in a field. It is about whether the cultivars you are growing or breeding still have the resistance you thought they did. When a new variant emerges, the situation can change very quickly,” explains Mogens Støvring Hovmøller.

Historically, monitoring has been organised at the national and regional levels. But wheat is grown on six continents, and rust spores can cross borders. If the same strain becomes established in several regions, it can therefore threaten cultivars and breeding lines on which many countries depend.

Each sample in the present study was linked to a specific time, location and host cultivar, enabling the researchers to track when particular rust types were first found in one region and later appeared elsewhere. Samples from different countries could therefore be analysed and tested under the same controlled conditions.

“We needed a place where we could gather samples from all over the world and examine them in the same way. Otherwise, it was difficult to determine whether rust found in different locations was actually the same strain with identical characteristics,” says Mogens Støvring Hovmøller.

The Global Rust Reference Centre (GRRC) at Aarhus University became a key part of a wider international network collecting data and analysing rust samples from Africa, Asia, Europe, Australia and South America.

The collaboration also developed standardised protocols, shared data formats and a database platform for visualising rust outbreaks at regional and global scales.

“This study could only be done because we have spent years building an international network in which samples are examined using comparable methods and data can be compared across countries and continents,” says Mogens Støvring Hovmøller.

Genetic traces revealed rust’s path across continents

The 3,240 samples were analysed using genetic markers – small variations in the genetic material that act as genetic identifiers. Where live samples were available, the researchers also tested them on wheat plants carrying different resistance genes. This enabled them to investigate both whether the rust samples were genetically related and which wheat cultivars they could attack.

“When we test the rust on plants, we can see what a new genetic variant can actually attack. This is where the monitoring becomes practically relevant, because you can link the variant to the cultivars and breeding lines that may be at risk,” says Mogens Støvring Hovmøller.

The most important methodological advance was the ability to analyse the fungus’s two nuclei separately.

“That became possible through our longstanding collaboration with the Australian National University. Previously, we could mainly see the combined genetic profile. Now we could begin to follow the individual nuclei and reconstruct where the hybrids came from,” says Mogens Støvring Hovmøller.

Rust fungi carry two nuclei side by side, each containing its own set of genetic material. Previously, researchers could mainly see only the combined genetic profile. Now they could investigate whether a new type of rust had acquired one nucleus from one known variant and the other from another.

“The breakthrough was that we were no longer limited to seeing only the combined profile of the two nuclei. We could assign genetic markers to the individual nuclei and thereby see which parents had contributed to the hybrids. Suddenly, we could reanalyse our entire geo-referenced dataset and see where and when hybridisation had probably taken place,” explains Mogens Støvring Hovmøller.

Two rust types can create a new variant on the same leaf

This exchange can occur when two strains of rust grow on the same leaf. The fungus spreads as microscopic threads, known as hyphae, through the plant tissue. When hyphae from different strains meet inside the plant, they may form a connection through which an entire cell nucleus can pass.

“When strains of very different origin meet on the same plant and exchange nuclei, a new variant may suddenly emerge that differs markedly from both parents,” says Mogens Støvring Hovmøller.

Finally, the genetic findings were compared with the timing of the first observations, the wheat-growing seasons, spore survival in the atmosphere and meteorological models. This analysis showed that the routes of spread varied. Between the Middle East, Europe and eastern Africa, windborne transport was a plausible explanation.

For the longest jumps, including those to Australia, the wind models could not explain the observed spread as well, making unintentional transport by people a more plausible explanation.

“We cannot always say exactly how a particular spore was transported. But when we combine genetic data, the timing of the first findings, plant tests and wind-dispersal models, we can determine the most plausible explanations,” notes Mogens Støvring Hovmøller.

Ten jumps between continents – seven followed by major epidemics

The study documented 10 cases in which specific types of rust had moved between continents. In seven of them, their arrival was followed by major epidemics in the new regions.

Australia illustrates how markedly the pattern has changed. Around 200 years passed between the beginning of European wheat cultivation in the country and the first recorded case of yellow rust in the late 1970s.

Over the past 10–15 years, however, researchers have recorded at least three, and possibly four, new introductions. At least two of these represented hybrids that were first detected several years before in Europe.

One of these hybrids, PstS10, was first detected in Europe in 2012 and the other, PstS13, in 2015. The analysis suggests that both inherited one nucleus from a rust strain that reached Europe from the Himalayan region in 2011. PstS10’s second nucleus came from a European variant already adapted to the region’s climate and wheat cultivars, whereas PstS13’s came from a strain that had arrived from the Middle East around 2006.

“This suggests that yellow rust is moving between continents far more frequently than before. However, our data do not allow us to calculate a single global rate for this development,” says Mogens Støvring Hovmøller.

“Normally, rust evolves through mutations – small changes at individual points in the pathogen genome. Here, however, roughly half of the genetic material is replaced at once. That can make the outcome far more difficult to predict,” explains Mogens Støvring Hovmøller.

One rust lineage came to dominate Europe

From a single rust sample found in Europe in 2012, the descendants of PstS10 spread to North Africa, the Middle East, Australia and South America. Today, they account for around 80% of the yellow rust samples that researchers collect from wheat in Europe.

“In 2012, we found a single isolate of the new hybrid. Today, its descendants – now comprising at least five new mutant races – have largely displaced much of the yellow rust previously found in Europe,” says Mogens Støvring Hovmøller.

Why PstS10 in particular became so successful is not yet fully understood. It has, for example, been found on wild grasses, which may suggest that it can infect a broader range of plants than many other yellow rust strains. The study cannot, however, determine whether this broader host range – or other characteristics – best explains its success.

The researchers also found evidence of similar exchanges of cell nuclei in other rust strains. One of these was PstS14, which, after it was first detected, accounted for all the samples analysed from northwestern Africa for three consecutive years. The results therefore suggest that PstS10 and PstS13 were not isolated cases.

Rust early warning gave Ethiopia time to respond

Another important finding came from Ethiopia, where the new genetic variant PstS16 was detected in December 2020. The strain, known as PstS16, had previously been seen only sporadically in South Asia. When new rust-infected wheat samples were submitted to the GRRC in spring 2021, PstS16 accounted for around half of those analysed from Ethiopia.

“When we tested it on wheat plants, we could see that PstS16 could attack many cultivars. We therefore asked our partners to collect more samples as quickly as possible, and when they arrived, half of them were PstS16. It was then clear that there was a reason to act immediately,” says Mogens Støvring Hovmøller.

Local authorities and the International Maize and Wheat Improvement Center (CIMMYT) were alerted, and fungicides were made available in case weather conditions became favourable for an epidemic. In addition, around 1,200 wheat lines from CIMMYT were tested in GRRC containment facilities in Flakkebjerg. The variant was able to attack a large proportion of the material intended for future cultivation.

The early-warning effort, which also involved spore-dispersal modelling by the University of Cambridge, enabled field-control measures to be prepared and breeders and authorities in Ethiopia and neighbouring countries to be alerted before PstS16 became more widespread.

New rust variants must be detected before the next growing season

The experience from Ethiopia shows the practical value of monitoring. The earlier a new rust strain is detected, the more time there is to test wheat cultivars under threat and to warn farmers and plant breeders before the next growing season.

“If you only realise that the disease pattern has changed once the epidemic has already taken hold in the field, major yield losses may occur before you understand what you are dealing with. Here, we were able to see almost from the outset where PstS16 came from and which cultivars might be at risk, giving us a chance to prepare before the variant became more widespread in East Africa,” says Mogens Støvring Hovmøller.

In Europe, researchers are now trying to link genetic monitoring to existing networks that test the value and sustainable use of new wheat cultivars. Small sets of wheat lines carrying different forms of rust resistance are planted at field-trial sites across Europe.

By observing infection levels and submitting samples with unusual disease patterns to national diagnostic laboratories and the GRRC, researchers can identify which resistance mechanisms the rust can overcome and link these traits to its genetic profile.

According to Mogens Støvring Hovmøller, such test sets have been sent to just under 100 trial sites this year. Researchers are also bringing together disease observations from several countries in a shared data system, allowing new findings to be displayed on maps and shared with researchers, advisers and plant breeders.

“Time is of the essence. If we discover something new in one season, we want to be able to report it before farmers and breeders must make decisions about the next one. Our work to build a global database and visualisation system for rust data has been essential in this respect,” emphasises Mogens Støvring Hovmøller.

Disease data are gathered through survey apps and displayed on interactive maps showing emerging rust strains, the wheat cultivars they affect and how they spread geographically. Part of this system is managed in Denmark through the Wheat Rust Early Warning programme at Aarhus University’s Department of Agroecology.

Monitoring must lead to more resistant wheat

The international monitoring programme is not only intended to track the rust strains that already dominate. The study also shows the value of detecting new variants as early as possible – especially if an aggressive hybrid emerges with the potential to spread across regions or continents. That gives plant breeders, agronomists and farmers more time to respond to a changing disease situation.

Once a dangerous strain has become established, fungicides may be needed to contain an acute outbreak. In the longer term, the aim is to feed the information gathered through monitoring into plant breeding, so that new cultivars become resistant to the rust strains that are on their way.

“Fungicides may be necessary in an emergency, but as far as possible, we prefer to breed our way out of the problem. That is why information about new types of rust must be incorporated into breeding work as quickly as possible,” says Mogens Støvring Hovmøller.

Establishing a global system is difficult, however. Seeds and rust samples must be transported safely between countries, and laboratories must have the necessary authorisation and facilities to investigate strains that are not yet present locally. The next step therefore depends not only on better analysis but also on a permanent international preparedness system.

For a crop that provides around one fifth of the world’s calories and protein, the stakes are high. New rust strains need to be detected, investigated and mapped before they can undermine the wheat cultivars on which a large part of the world’s food supply depends.