Study shows surgical precision employed by pathogen in this process

Ustilago maydis attacks and reproduces in the aerial parts of the maize plant. A huge tumor-like tissue growth often forms at the web-site of the infection. These galls can grow to the size of a child’s head. The growths are triggered by molecules released by the fungus, called effectors. They manipulate the plant’s metabolism and suppress its immune system. They also promote cell growth and division in corn. They do this by interfering with a plant signaling pathway regulated by auxin, a plant hormone.

“The fungus uses this signaling pathway auxin for its own purposes,” explains Professor Armin Djamei, who heads the Department of Plant Pathology at the INRES Institute at the University of Bonn. “This is because the enormous tissue growth devours the energy and resources then lacking to defend against Ustilago maydis. Additionally, the fungus finds an ideal supply of nutrients in the growths and can multiply well there.” The formation of the characteristic galls is therefore in the interest of the pathogen.

“We therefore wanted to know how the fungus promotes these proliferation processes”, explains Djamei. “To do this, we searched for genetic material in the fungus allowing it to control its host plant’s auxin signaling pathway and therefore its cell growth.” The complex research began seven years ago at the Gregor Mendel Institute in Vienna. Later, the culture researcher continued his work at the Leibniz Institute in Gatersleben and later at the University of Bonn.

The pathogen reprograms its host

Successfully: Together with his collaborators, he was able to identify five genes that the fungus uses to manipulate the host plant’s auxin signaling pathway . These five genes, called Suggestion1 to Suggestion5, form what is called a cluster: if we imagine the entire genome of Ustilago maydis as a thick encyclopedia, these five genes are somehow found on successive internet pages.

Genes are development manuals — the fungus needs them to produce the respective proteins. “The proteins encoded by the five Idea genes can bind to a maize plant protein known to experts as Topless,” says Dr. Janos Bindics. A former employee of the Gregor Mendel Institute, he and his colleague, Dr. Mamoona Khan, performed many of the study’s key experiments.

Topless is a central switch that removes very different signaling pathways in the plant. Fungal effectors produced by the five Suggestion genes override this repression — and do so very specifically for signaling pathways that benefit the fungus, such as the auxin-induced growth signaling pathway. On the other hand, the other signaling pathways controlled by Topless are not affected. “In a figurative sense, the fungus works with surgical precision,” Djamei points out. “It does exactly what it needs to do to best infect the corn plant.”

Views for basic research

There are a number of pathogens that interfere with the auxin signaling pathway of the hosts they infect. Exactly how is often not fully understood. Topless may also play a crucial role in this process in other cultures. After all, the protein originated hundreds of millions of years ago and its central role has hardly changed since then. It therefore exists not only in maize, but in a similar form in all other terrestrial plants. For example, researchers were able to show that the Tip effectors of Ustilago maydis also interfere with the auxin signaling pathway of other plant species.

The results could therefore help to better understand the infection processes in the main plant diseases. The results are of particular interest for basic research: “Thanks to them, it will be possible for the first time to influence specific effects of the auxin signaling pathway in a very targeted manner and thus to elucidate even more precisely the effect of these important plant hormones,” hopes Armin Djamei, who is a member of the “Sustainable Futures” transdisciplinary research space and the PhenoRob center of excellence at the University of Bonn.

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