Switching from harmful to helpful fungi

When your fresh strawberries go fuzzy with mold, or grapes turn gray and shrivel at the bottom of the fruit bowl, it's always a bit disappointing and unpleasant. The culprit is typically a disease-causing fungus calledBotrytis, which devastates food crops globally and is easily spread by wind and soil. However, there are many fungi which have a less destructive relationship with their host plants, even forming partnerships which can help the plant to thrive. Promoting the beneficial traits of fungi and suppressing undesirable outcomes (like moldy fruit) would greatly aid global food security and help reduce a huge amount of food waste.

"Plant-associated fungi show varied infection lifestyles ranging from mutualistic (beneficial) to pathogenic (harmful) depending on the host enviroment. However, the mechanisms by which these microbes transit along these different lifestyles remain poorly understood," said Associate Professor Kei Hiruma from the Graduate School of Arts and Sciences at the University of Tokyo. "We analyzed genetic information from varied strains of a root fungus calledColletotrichum tofieldiaeusing comparative transcriptomic analysis, which enabled us to study differences in gene expression between each strain. Surprisingly, we found that a single fungal secondary metabolism gene cluster, called ABA-BOT, solely determines whether the fungusexhibits pathogenic or mutualistic traits toward the host plant."

Colletotrichum tofieldae是一种真菌,植物当t通常好处hey suffer a phosphorus deficiency, helping them thrive despite the lack of this vital nutrient. It has even been shown to increase the growth and yield of economically important crops such as maize and tomatoes. In this study, the multi-institutional team used thale cress as the host plant and sourced six strains ofCtfrom different geographical locations to infect it with. Five strains significantly promoted plant growth, as expected, but a sixth -- calledCt3-- was found to suppress nutrient uptake, inhibiting plant growth and leading to symptoms of disease. So, what caused this drastic change?

"We identified two key points: First, on the fungal side, thatCt3activates the ABA-BOT biosynthesis gene cluster; and second, on the plant side, thatCt3induces the host plant's ABA signaling pathways, through which the fungus inhibits plant growth," explained Hiruma. The researchers found that both pathogenic and mutualistic strains ofColletotrichum tofieldaecontain the ABA-BOT gene cluster, but mutualistic strains did not express it, i.e., the genes were not activated. The discovery came as a surprise, as conventionally pathogens and mutualists were thought to have distinct characteristics, but these findings suggest that they are more intricately related.

When the gene cluster was disrupted, either at a genetic level or by changing the plant's environment, theCt3was rendered nonpathogenic and even became beneficial to the host, promoting root growth. Although further study is needed, it appears that the ABA-BOT gene cluster may contribute to pathogenesis in diverse fungi beyond theCtspecies. For example, it may be involved in the pathogenesis of theBotrytiswhich afflicts our household fruit and vegetables. "If we gain a comprehensive understanding of the regulatory mechanisms governing the fungal secondary metabolism gene cluster, we can devise a method to selectively suppress potential pathogenesis in otherwise beneficial fungi, optimizing their utilization in agriculture and harnessing the full potential of the microbial diversity naturally present in soil ecosystems," said Hiruma.

"I have come to realize that even pathogens can exhibit nonharmful characteristics during a significant portion of their life cycles. In fact, I am beginning to contemplate the possibility that what we traditionally refer to as pathogens may actually function as beneficial microbes under other conditions."