Genetic defenders protect crops from fungal disease

Like waves of soldiers guarding a castle gate, multiple genetic defenders cooperate to protect plant cells against powdery mildew disease, according to a new study. Powdery mildew is a common fungal infection in plants that attacks more than 9,000 species, including many crops such as barley and wheat, and horticultural plants such as roses and cucumbers. The researchers, including Shauna Somerville and Mónica Stein of the Carnegie Institution’s Department of Plant Biology, are the first to document how these defense genes team up in plants. The discovery could help combat fungal parasites that devastate crops and cost growers billions of dollars in pesticides every year.

The study, published in the November 18 issue of the journal Science, describes powdery mildew infection in the mustard relative Arabidopsis thaliana. Each species of mildew is host-specific, meaning it can infect some plant species, but not others. By disabling protective genes in Arabidopsis, the researchers were able to infect the plants with species of powdery mildew that normally attack peas or barley, revealing much about how plants use genes to fight infection.

“Most plants are resistant to the majority of pathogens they encounter, but the basis for this resistance was unknown,” Somerville said. “Identifying these genes has provided us with the first insight into how plants defend against multiple pathogens.”

Once a powdery mildew infection takes hold, it covers the plant with fuzzy splotches, while sapping precious nutrients. At the cellular level, the fungal spores invade healthy plant cells and form root-like feeding structures called haustoria. The plant cell wall is the primary barrier to this invasion and one of the defense genes described in the current study, called PEN2, prevents the fungus from penetrating cell walls in the first place.

If this first line of defense breaks down, as it does in about 5 to 25 percent of normal Arabidopsis plants (depending on the mildew species), a second set of genes jumps into the fray. These genes, called EDS1, PAD4, and SAG101, work together in a complex inside the cell, and can signal infected cells to die. By sacrificing these fallen cells, the defense genes can spare healthy ones from infection.

Somerville, Stein, and colleagues at the Max Planck Institute for Plant Breeding in Köln disabled the protective genes in Arabidopsis by introducing mutations, one at a time and in various combinations. They infected these mutants with one of two species of powdery mildew: Blumeria graminis hordei, a species that attacks barley, and Erysiphe pisi, one that thrives on the leaves and pods of pea plants.

“Disabling just three genes allowed the pea powdery mildew to reproduce as well on Arabidopsis as it does on its normal host,” Somerville remarked. “Thus, the resistance barriers limiting the growth of inappropriate pathogens are much less complex than expected, relying on just a limited number of genes.”

The EDS1, PAD4, and SAG101 gene complex’s ability to signal cell death is relatively well known to scientists. However, very little is known about how PEN2 behaves in the cell. The current study demonstrates that the PEN2 protein is a catabolic enzyme–a protein that breaks down other molecules–though its specific target remains unknown.

The study expands on the researchers’ previous work with a gene called PEN1. As its name suggests, PEN1 and PEN2 seem to share a common purpose. However, they seem to act via different mechanisms, and PEN2 protects against a wider range of fungal pathogens. For example, Arabidopsis plants with a disabled PEN2 gene are also more susceptible to Phytopthora infestans, the fungus responsible for the notorious Irish Potato Famine of the mid-19th century.

“The resistance mechanisms operating at the cell wall seem to be surprisingly simple,” Somerville said. “This suggests it might be possible to reverse engineer crops like wheat with Arabidopsis PEN genes to help control powdery mildew and other destructive diseases, thus minimizing the need for pesticides.”