Durable Rust Resistance in Wheat
Background and Rationale
Stem Rust: Historical Perspective
Stem rust is the most feared disease of wheat. Stem rust spores arriving as late as one month before harvest can turn a previously healthy crop into a tangled mass of stems, which produces little to no grain. Moderately infected fields can produce as many as 1011 spores/hectare, many of which are picked up by wind currents. The result is that astronomical numbers of rust spores can be moved hundreds or thousands of kilometers to infest other regions. In the 1953 pandemic in North America, rust spores produced in fields in Kansas were deposited across 100,000 km2 of wheat 1,000 km north in North Dakota and Minnesota at a rate of over eight million spores per hectare. The result was loss of 40% of North America’s spring wheat crop. Although individual fields can be annihilated, on a regional basis, average yield losses under epidemic conditions are commonly 10%, enough to have disastrous humanitarian effects on wheat producing countries in the developing world, as well as substantial secondary impacts on the entire global economy. Pandemics have been noted throughout history, with significant events occurring in South Asia, China, Central Asia, East and Central Europe, North America and elsewhere in the past 130 years. The last major continental pandemic was that described above in North America. The episode triggered international collaboration that helped lay the groundwork for the Green Revolution wheats. Although stem rust epidemics have occurred since 1955, they were relatively localized (e.g. 1973 and 1974 in Australia and the SE United States, respectively; and 1992 in Ethiopia). This 40-year period where stem rust was largely quiescent is a result of genetic resistance.
Genetic resistance to stem rust has been a priority objective of wheat breeders for over 100 years. The period between 1900 and 1955 saw the discovery and deployment of various major resistance genes, which are sufficiently potent that they can preclude stem rust spore production even if a plant possesses only that single gene. Their hallmark phenotype is the hypersensitive response. These genes are “race specific” and function only if the infecting population of stem rust is a race that lacks “virulence” to that specific wheat resistance gene. They are also known as “seedling resistance genes” because their presence and identity is determined by seedling assays (note that this type of gene also imparts resistance to adult plants where resistance is needed to prevent yield loss).
From 1955 onward, most of the world’s wheats, including the Green Revolution varieties, were protected by both seedling resistance genes and a second class of resistance genes that only function in the adult stage. These genes are referred to as adult plant resistance (APR) genes. APR is generally considered to be race non-specific and dependent on several genes, each with minor, additive effects.
Before 1955, stem rust resistance was not effective over time (i.e., durable) because the pathogen was able to spawn virulent races rapidly, which “defeated” the race-specific genes upon which resistance was based. Wheat production was in a continual boom-bust cycle where a variety seemingly unaffected by stem rust in one year was annihilated the next. This boom-bust phenomenon as it relates to wheat stem rust is not a product of modern plant breeding—experts believe that some Biblical references to plagues refer to stem rust. The past 60 years have witnessed expanded wheat production and productivity, yet stem rust has not been a significant problem.
In that same period, wheat improvement specialists continued to improve wheat for many other characteristics and together with improved agronomic practices, wheat scientists and farmers have kept wheat supply moving in step with increasing demand the past four decades. Partly because of these successes, two critical features of a resilient wheat improvement system were allowed to decay:
- the capacity (human and infrastructure) to work with stem rust; and
- the release frequency of varieties with durable, race non-specific stem rust resistance.
A third factor—a robust collaborative international network of wheat improvement institutions and scientists—has also atrophied.
In 1998 a Ugandan crop scientist collected samples of a stem rust variant that appeared to be virulent on the previously undefeated and widely used major gene Sr31. The sample was multiplied on universal susceptible wheat and then used to challenge a series of wheat stem rust genes in a process called pathotyping. This bioassay demonstrated that the Uganda isolate represented a unique pathotype (or race), which had a unique and potentially dangerous virulence pattern. In formal terms, this race is designated TTKS, but it is widely known by the name given the isolate: Ug99 (“Ug” for Uganda; “99” for the year its discovery was published). By 2004 Ug99 had colonized wheat fields of both Kenya and Ethiopia. An expert panel report, “Sounding the Alarm on Global Stem Rust,” issued May 29, 2005, unequivocally declared Ug99 to be a threat to world wheat production (see www.globalrust.org). The report predicted that Ug99 would migrate across the Red Sea to Yemen, then to the Middle East, and subsequently to Central and South Asia. The predicted immediate path of Ug99 to South Asia covers a region that produces 19 percent of the world’s wheat (ca. 117 million tons) with a population of one billion people. It is likely that either wind currents or inadvertent transport will eventually carry Ug99 to North Africa, Europe, West Asia, China, Australia, and the Americas.
Collaborative research since early 2005—under the umbrella of the CIMMYT (International Maize and Wheat Improvement Center) and ICARDA (International Center for Agricultural Research in Dry Areas)-led Global Rust Initiative (GRI), initiated by Dr. Norman E. Borlaug—has established that Ug99 defeats virtually every race-specific resistance gene used in commercial varieties grown throughout the world. Ug99 defeats more of the 50+ known major resistance genes than any previously known stem rust lineage. In 2006, researchers discovered in Kenya a variant of Ug99 that defeats the widely used stem rust gene Sr24. This even more dangerous race will follow the same path that Ug99 is on. Over 90 percent of the world’s commercial wheat varieties are susceptible to the new variant, including almost all the wheat on the predicted path between East Africa and South Asia. Without swift intervention, stem rust will re-establish itself as a chronic cause of lost production in vast tracts of wheat in the developing world.
In January 2007, it was confirmed that Ug99 had migrated from eastern Africa and was infecting wheat in Yemen in the Arabian Peninsula. Scientists are convinced that the Ug99 lineage will reach the Middle East in the immediate future.
Potential Impact of Ug99 on the World’s Poor
Wheat represents approximately 30% of the world’s production of grain crops. The FAO predicts that 598 million tons of wheat will be harvested this year on 220 million hectares of land. Nearly half of that production will be harvested in developing countries. On average, each person in the world consumes 68.2 kilograms of wheat each year. That equates to about 630 calories per day per person, or 1/2 to 1/3 of the minimal energy requirements of most adults. In West Asia, North Africa, and Central Asia, wheat provides more calories than all other grains combined. The Middle East and North African countries consume over 150% of their own wheat production and are thus heavily dependent on imports.
Once Ug99 and its derivatives have established themselves in North Africa, the Middle East, and South Asia, annual losses could reach US$ 3 billion in any given year. The effects on rural livelihoods and geopolitical stability would be incalculable. Large populations of poor wheat-growing farming families would be seriously affected and few would have alternative livelihoods. The impact on landless laborers dependent on agricultural jobs would also be severe, and one could anticipate an increase in the rural-urban migration of landless laborers and small farmers. Moreover, such large production losses would have significant implications for rural and national economic growth rates in seriously affected countries and could even affect global wheat markets.
The Green Revolution introduced semi-dwarf wheat varieties developed in Mexico by Nobel Laureate Dr. N.E. Borlaug to various developing countries during the 1960s and 1970s. It not only helped feed the world at a time of impending famine but also triggered an industrial revolution in subsequent years. Increased crop production did not come just from the semi-dwarfs’ high yielding ability and higher input efficiency but also from their genetic resistance to the rust diseases. This resistance has saved billions of dollars annually by avoiding devastating epidemics that would have had major effects on global food supply and prices.
Were it not for rust resistant wheat varieties, resource-poor farmers who cannot afford pesticides would still be at the mercy of such epidemics. The best control strategy for poor farmers in the developing world—and the most environmentally friendly and profitable strategy for commercial farmers everywhere—is to grow genetically resistant crop varieties. To give an example, protecting one hectare of wheat from stem rust disease in the highly productive Nile Valley of Egypt would require two applications of fungicides, at a cost of US$ 80. This lost income is equivalent to 8-10% of wheat productivity in the area, which stands at about 6 tons per hectare. Fortunately, cultivation of resistant wheat cultivars has avoided the excessive use of chemicals in about two-thirds of the 220 million hectares sown to wheat worldwide. Use of resistant varieties thus increases profit margins, helps keep the prices of staple crops at affordable levels, and has a beneficial effect on human health because fewer agrochemicals are applied.
Fortunately, Ug99 does not defeat all known major genes, and recent research in East Africa shows that minor-gene-based adult plant resistances are also effective. These resistances can and must be bred into varieties that exhibit performance and quality characteristics that will enable their acceptability to farmers. Phenotyping breeding progeny for response to the Ug99 lineage must be done in East Africa today for bio-security reasons (the migration is as of yet limited); and in future because East Africa is likely to be a breeding ground of new stem rust variants for the foreseeable future. Intensifying the International Centers’ wheat improvement programs to enable maintenance of yield gains while including stem rust resistance in the profile of previously required characteristics (including resistances to leaf and yellow rusts) will generate Ug99 resistant varieties for much of the immediate threat area. Aggressive variety testing and multiplication tactics must be pro-actively encouraged to ensure availability of seed. An under-utilized developing country wheat research network must become reacquainted with a dangerous foe that many have not ever seen. The migration and evolution of Ug99 and its inevitable derivatives must be monitored to provide scientists information on which genes or gene combinations remain effective and to inform policy makers about choices in research investments, plant protection, etc. Prudence dictates we engage in targeted searches for additional resistance genes while simultaneously employing cytogenetic and molecular marker technologies to improve the utility of effective genes, and to develop tools that will speed their deployment in farmer’s fields.
In a longer term approach, we propose to exploit the rapidly expanding body of knowledge of plant host-pathogen interactions, coupled with the availability of specialized genetic resources in rice, to search out paths to unraveling the mystery of why wheat succumbs to rusts and rice and some other species do not.