Something odd happened in the wheat fields of Australia and Africa in the forties of the last century: yellow or brownish spots of dead tissue were suddenly observed on the plant leaves. It was soon discovered that this phenomenon was associated with infestation by Pyrenophora tritici-repentis – a fungus that had been known since the turn of the previous century but had until then been harmless. However, this harmlessness became increasingly a thing of the past. The spots often became darker and wheat tan spot, as the disease was now called, became widespread. In 2003 it was the most frequent wheat disease in Canada, and according to a study from Germany in 2004 the yield of wheat grain in our neighbouring country shrank by 10 to 36 percent because of the fungus.

The corresponding research increased in parallel with the increase in the disease. It revealed that the fungus develops its harmful effect via the substance ToxA. An additional finding showed that only wheat plants carrying the Tsn1 gene are sensitive to the toxin. But how on earth did the fungus happen to mutate into a pest? This question was also answered recently: it was not a classical gene mutation. Instead Pyrenophora tritici-repentis (Ptr) acquired the gene for ToxA from Stagonospora nodorum (Sn), a fungus that also occurs in wheat. This conclusion was reached by ETH researchers Bruce McDonald and Eva Stukenbrock from the Institute of Integrative Biology together with colleagues from the USA and Australia (1). The study, which is the first to show horizontal gene transfer in fungi, appears in the new issue of Nature Genetics (2).

Uniformity is evidence of a historically recent event

The new study began with a genome project on Sn, the fungus that causes the wheat disease called leaf blotch and which has been known since the late 19th century. While Richard Oliver from Murdoch University in Australia was scanning the list of 17,000 fungal genes he noticed No. 16571, which stood for a gene very similar to the ToxA gene of Ptr. This was unexpected, since nobody had previously suggested that ToxA is also present in Stagonospora. In collaboration with Tim Friesen of the US Department of Agriculture it was also discovered that ToxA is necessary in both fungi to enable them to cause disease in wheat plants that have Tsn1 genes.

With these suspicious factors as a starting point, Bruce McDonald and Eva Stukenbrock examined their collection of Sn and Ptr. It became apparent that among about 800 fungus isolates originating from the whole world, 80 percent of the Ptr and 24 percent of the Sn contained ToxA. At the same time, the ToxA genes in Ptr were practically identical, but were highly variable in Sn. The researchers also discovered that the flanking sequences of the ToxA genes were very similar in both fungi and were reminiscent of genes called transposons, which are responsible for the asexual transfer of other genes.

The fungus Pyrenophora tritici-repentis causes brown spots on wheat plant leaves. ETH researchers discovered how the fungus turned into the pathogen causing wheat tan spot.

Taken together, these findings represent the first proof of horizontal gene transfer in fungi. They also explain the sudden emergence of wheat tan spot in the middle of the last century. “The uniformity of the ToxA gene in Pyrenophora contrasts with the variability of the other genes of this fungus,” explains Bruce McDonald. In this respect gene transfer is a better explanation than a genetic bottleneck in the history of Ptr, which would have had to act on all the genes. The researcher explains the high frequency of 80 percent in Ptr by the fact that ToxA greatly helps Pyrenophora to spread. It would be possible to test this hypothesis by looking to see whether fungal strains with ToxA occur mainly in regions where the wheat carries the Tsn1 gene.

The next target: how do fungi transfer genes?

If such a connection were proven, it would then be possible to advise plant breeders to eliminate the Tsn1 gene, says McDonald. “However, our study does not yet result in any direct application to farming practice.” Nevertheless, in hindsight a change in wheat field cultivation that was regarded as permanent can be said to have had adverse consequences. For example allowing straw and other residues to remain on the ground after the wheat harvest probably protects against soil erosion, but at the same time this procedure promotes the spread of Prt. On the situation in Switzerland, Bruce McDonald comments that, “Farmers in this part have been spared wheat tan spot because many of them still plough their fields. By doing this they also remove the wheat stubble on which the harmful fungi survive to the next generation of wheat.”

However, considerations of agricultural practice are not the researcher’s main priority. Having shown that horizontal gene transfer occurs in fungi, he now wants to find out how it takes place. It is suspected that tubular interconnections between fungal spores and known as conidial anastomosis tubes play a part. This is because they have been observed in the case of Ptr and Sn present on the same wheat plant. Once horizontal gene transfer in fungi has been explained, there is a better chance of assessing whether awkward genes can be transferred in this kingdom of living organisms as easily as they can in bacteria and viruses.