New research shows how rust robs plant cells

CSIRO Plant Industry researchers have identified the molecular skeleton key that allows rust fungi -- ubiquitous pathogens of cereal and horticultural crops around the world -- to burgle plant cells.

Their discovery presages an age in which molecular geneticists may be able to custom-design resistance genes to protect crops against 'breakthrough' rust fungus mutants, like the virulent new strain of stripe rust that swept through the eastern Australian wheat belt last year.

The long-sought 'avirulence' gene, identified in a strain of flax rust, encodes a protein that appears to be essential to the infection process, according to team leader Dr Peter Dodd.

The CSIRO team identified the gene by comparing gene-expression profiles in virulent and non-virulent strains of flax rust.

In the evolutionary arms race between rust fungi and their host plant species, plants have evolved an effective counter-measure.

The so-called avirulence genes of rust fungi somehow interact with proteins encoded by complementary resistance genes in the plant host. The reaction initiates a necrotising response that sacrifices healthy tissues surrounding the infection site, quarantining the pathogen within a small spot of dead tissue.

According to CSIRO, rust-resistant wheat varieties save the Australian wheat industry some AUD$300 million a year in lost production.

Rust-resistance genes impose strong selection pressure for mutations that modify the avirulence gene so it no longer detectable by the corresponding resistance gene, or genes.

Such mutations create 'breakthrough' rust strains that can cause devastating infections in plants protected by single, dominant resistance genes. But breeders incorporate multiple resistance genes in cultivars, whose additive effects mean that loss of resistance is usually only partial.

Wheat and barley breeders are usually able to identify new sources of resistance and incorporate them in breeding programs.

The new stripe rust fungus, which first appeared in WA crops in 2002, appears to have been inadvertently introduced by someone who had recently visited the US. It forced wheat breeders to cull formerly resistant cultivars that had become susceptible to infection, causing substantial damage to long-term breeding programs.

Dodd said his team has identified between one and three avirulence genes in different strains of flax rust, and there is considerable variation between rust strains. "They don't resemble any other genes in plants," he said.

He said his team's findings supported the hypothesis that avirulence genes are indispensable to the fungi, and there is strong selection pressure for new mutations that, in breakthrough strains, effectively render their products invisible to the plant host.

Dodd said the invading fungus extends filament-like hyphae into the air spaces between cells, and makes contact with the cell surfaces via pad-like extrusions called haustoria.

The cells of the haustoria appear to secrete the avirulence protein, which passes through the cell membrane into the cell's interior, where it is detected by the corresponding resistance gene's 'alarm' protein.

"If resistance genes were highly conserved, it would be difficult for the rusts to change them in response to the evolution of new resistance genes in the host plant," Dodd said. "But the high variability in avirulence genes between rust strains suggests they evolve rapidly. In the short term, if we can work out how the plant cells recognise the proteins from avirulence genes, we can help breeders identify which genes they should be incorporating in new cultivars.

"But we still need a lot of basic research into how the recognition reaction occurs."

Dodd said the challenge would then be to identify how mutations in avirulence genes allow virulent new rust strains escape detection. It may then be possible for molecular geneticists to custom-design resistance genes to provide durable resistance against new rust strains.