Pathogen capitalizes on ancient relationship

Catherine Jacott of the John Innes Centre said the results of the full scope of the research will have important implications for crop improvement by enhancing beneficial mycorrhizal fungi interactions while reducing crop losses from powdery mildew. | Supplied photo

A gene that allows plants to reap the benefits of a mycorrhizal fungi also makes them susceptible to powdery mildew

If the mildew locus O gene causes crops to be susceptible to powdery mildew, why have plants hung onto this seemingly detrimental genetic relationship over evolutionary history?

Unravelling this enigma has been the goal of scientists at the John Innes Centre in the United Kingdom and the Shanghai Institute of Plant Physiology and Ecology in China. In play are four biological elements — the plant, the MLO gene, arbuscular mycorrhizal (root) fungi, and the powdery mildew pathogen, which is a fungal pathogen that infects many plant species and can cause significant crop losses.

This relationship goes back millions of years.

The MLO gene is found in a variety of plants including economically important crops like wheat, rice and legumes.

While the gene contributes to the plant’s natural processes, the scientists found it is especially beneficial to the mycorrhizal fungi and, by default, the powdery mildew.

“We do not yet know what processes MLO regulates that enable both mildew infection and fungal mycorrhization,” said Catherine Jacott of the John Innes Centre. “One hypothesis is that MLO suppresses defence to allow mycorrhization, and powdery mildew has exploited this suppression of defence to facilitate their infection (of the plant). Another hypothesis is that MLO activates specific processes to enable mycorrhization, and powdery mildew requires similar processes to facilitate its infection.”

It has been known for some time that the MLO gene causes major crops to be susceptible to powdery mildew and that the loss of the gene (or removal through selective breeding) generates a stronger resistance against the pathogen.

In the study, some mutant plants of barley, wheat and a small legume called barrel clover native to the Mediterranean were devoid of the MLO gene. While this allowed the plant a greater defence against powdery mildew, the downside was that there was a decrease in the activity of many key genes needed to facilitate the mycorrhizal fungi establishing itself inside the plant’s root cells. The researchers concluded that while the primary role of MLO in flowering plants was to aid establishment of the root fungi, the role had been hijacked by powdery mildew.

“The MLO gene has been removed (mutagen-induced MLO mutants) for use in barley breeding since the 1940s to provide resistance to powdery mildew,” said Jacott. “However, in these cultivars, MLO is removed in the entire plant, therefore potentially affecting mycorrhizal colonization of roots. Since mycorrhizal fungi and powdery mildew, respectively, infect root and shoot, it may be possible to generate genotypes that could fully support mycorrhiza while remaining non-hosts for powdery mildew (removing MLO just from leaves). However, in practice, this kind of genetic modification is difficult and so unlikely (yet) to be undertaken.”

However, much more is needed to be understood about the complexity of the relationship between the plant, the gene, the fungi and the powdery mildew.

“We do not yet know how MLO is activated by the mycorrhizal fungi or what downstream processes MLO activates to enable the fungi’s colonization (in the roots),” she said. “We are researching molecular mechanisms underlying the reduced mycorrhizal colonization in MLO mutants, i.e. identifying genes affected by MLO, which influence mycorrhizal colonization. We would also like to research what activates MLO during these plant-microbe interactions. Is it by the fungi or molecules (called effectors) released by the fungi?

“In addition, we want to research the effects of mutations in MLO on mycorrhizal growth responses. How does delayed mycorrhizal colonization in MLO mutants affect plants over their lifetime in the field?”

She said that the results of the full scope of the research will have important implications for crop improvement by enhancing beneficial mycorrhizal fungi interactions while reducing crop losses from powdery mildew. Improved understanding of the root microbiome will be of great value for breeders developing future crop plant initiatives.

“I have presented my work to crop farmers during crop breeding outreach events and workshops,” said Jacott. “Farmers are interested in the potential of using mycorrhizal fungi to help provide nutrients to crop plants and reduce the use of polluting fertilizers.”

The study was recently published in the journal New Phytologist.

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