Famine in Africa and the Middle East? Devastating stem rust fungus threatens global staple crop, but genomic solution may finally be on the horizon

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Wheat helps feed the world. It grows well in temperate climates and its grains are an excellent source of starch, protein, fiber, B vitamins and more. Among cereal grain production, wheat is second only to corn: In 2019, farmers were expected to grow about 767 million metric tons of the stuff, according to the Food and Agricultural Organization of the United Nations.

Yet over the past two decades, a growing threat has attacked wheat production in Africa, and could in time decimate wheat harvests around the world. The scourge — known by the innocuous name Ug99 — is a strain of the stem rust Puccinia graminis f. sp. tritici. Stem rusts are fungal pathogens that parasitize wheat, but Ug99 is particularly effective at decimating whole fields. It is also spreading rapidly after appearing to be contained.

Crops affected by stem rust are often entirely destroyed, and until the 1950s, the fungus was able to wreak havoc on agriculture across the globe — including in the United States. Researchers eventually managed to identify strong resistance genes against the fungus, and successfully bred those genes into new plant varieties beginning in the 1960s, leaving the fungus contained and all but forgotten.

A generation later, however a new strain of wheat stem rust appeared — this time in Uganda, in 1998. This new strain, called Ug99 (Ug for the country where it was first discovered, 99 for the year when it was officially named), was immune to most of the known resistance genes. By 2010, it had emerged as a global threat and is now found in wheat fields across Africa and the Middle East, and shows signs of spreading farther. Ug99’s global spread could devastate wheat production and trigger famine.

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Food and Agriculture Organization of the United Nations

“Since this fungus is airborne it is very difficult to limit its spread,” said Dr. Benjamin Schwessinger of Australian National University. “Rust isolates from South Africa have migrated to Australia, likely through wind patterns.”

Wheat overwhelmed

About 80 to 90 percent of today’s wheat strains are susceptible to Ug99, said Dr. Schwessinger. Research has identified some of the genetic underpinnings of Ug99’s deadly talents — such as its ability to infect wheat strains containing Sr31, a resistance locus affective against other stem rust isolates. But Ug99 is spreading at a fast pace, and scientists need a quicker pipeline to study the strain’s genetic and molecular properties.

Dr. Schwessinger is part of a team of researchers from the United States, South Africa and Australia that recently employed a genome-wide approach to investigate Ug99’s provenance and virulence. The group, led by Dr. Melania Figueroa and Dr. Peter Dodds at Australia’s  Commonwealth Scientific and Industrial Research Organisation (CSIRO), set out to assemble chromosome-length reference genomes for Ug99 and Pgt21-0, an older stem rust strain from Africa.

Their efforts uncovered genomic evidence for Ug99’s surprising origins, as well as potential genetic vulnerabilities that researchers could exploit to breed resistant wheat strains — achievements all the more remarkable given a major genomic complication: Stem rusts, like many fungi, have two haploid nuclei per cell. “Traditional next-generation sequencing methods could not easily discern which scaffolds belonged to which nucleus” commented joint first author of the publication, CSIRO scientist Dr. Narayana Upadhyaya.

The team began by generating reads on Illumina and PacBio platforms. After assembling and collapsing reads into scaffolds for both Ug99 and Pgt21-0, the team discovered something unexpected: half the scaffolds in Ug99 and Pgt21-0 were more than 99 percent identical. The two strains appeared to share half their genome.

Hi-C forensics

The roughly half-genome’s worth of sequence that was common between Ug99 and Pgt21-0 could be a sign of shared ancestry. But unlike people, who have just one route to pass genetic information to the next generation, stem rusts and other fungi with multiple nuclei have several reproductive options. Growing on wheat, stem rusts can reproduce via asexual spores for generations. They can also undergo sexual reproduction, though that requires an intermediate host, the common barberry. Scientists have also uncovered evidence hinting that strains could exchange nuclei.

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To divine among these possibilities, the team turned to Phase Genomics to assign scaffolds to their nucleus of origin within each strain. They generated Hi-C libraries for Pgt21-0, which they used not only to create a chromosome-length assembly, but also assign chromosomes to each of the two nuclei.

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From Hi-C to hyphae

This complete, nuclear-sorted assembly revealed that Ug99 and Pgt21-0’s shared sequences aren’t a mixture of the two nuclei as expected for sexual reproduction. Instead, the common sequences were confined to a single haploid nucleus. That key conclusion indicates that Ug99 likely arose through “somatic hybridization,” in which hyphae from different strains fuse and exchange nuclei. Since one nucleus in Ug99 so closely resembles Pgt21-0, it likely came from a Pgt-like strain.

“We were not expecting this at all,” said Dr. Figueroa. “It was one of those amazing moments in science when you stop and think how much there is still to learn about nature.”

By pairing two haploid nuclei from different genetic lineages, a somatic hybridization event in stem rusts can instantly create new combinations of alleles without sexual reproduction and meiosis. This may explain Ug99’s sudden emergence in the 1990s, as well as why most wheat strains are vulnerable to infection: Ug99’s unique genetic makeup is too divergent from the more established stem rust strains that have been around for decades or longer.

“There are ramifications of such a big discovery, such as what this means for disease management and pathogen surveillance,” added Dr.Figueroa.

Join the Resistance

The team has already started to mine the Ug99 and Pgt21-0 genomes for information that could help scientists decipher the details of Ug99’s virulence and breed countermeasures into vulnerable wheat strains. They confirmed past research indicating that Ug99 is a heterozygous carrier of AvrSr35 and AvrSr50, two dominant factors that activate anti-rust immune responses in wheat. These and other loci may be immunological routes in wheat that researchers could exploit. In addition, the completeness of the Ug99 and Pgt21-0 genomes will help researchers find more loci like these explains Dr. Dodds. These resources will also make it easier to survey the genetic diversity — and the movement of nuclei — among stem rust populations, and may help scientists identify the strain that gave Ug99 its second nucleus.

Together these tools could ensure that Ug99’s departure is as abrupt as its arrival — and give wheat, one of our most important staple crops, some much-needed relief.

This research was supported by the 2Blade Foundation, USDA-Agriculture and Food Research Initiative (AFRI) Competitive Grant (Proposal No. 2017-08221), an USDA-NIFA Postdoctoral Fellowship award (2017-67012-26117), an ARC Future Fellowship (FT180100024) and the University of Minnesota Lieberman-Okinow and Stakman Endowment.

Kaylee Mueller, a product marketing manager at Phase Genomics, a biotechology company that addresses the impact of genetics on society, often writes about genomics and metagenomics. Follow her on Twitter @Kayleezyme

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