It’s a fine line; bacteria can be an enemy or ally to plants

September 06, 2023

Discovery of molecular mechanisms that separate the contrasting strategies of filamentous fungi: symbiosis and parasitism

A research group from the University of Tokyo, Hokkaido University, RIKEN CSRS, Research Center for Medicinal Plant Resources, and Nara Institute of Science and Technology found that a single fungal secondary metabolite biosynthetic gene cluster in endophytic fungi (molds) establishing in plants supports a diverse and continuous infection strategy—from symbiosis to parasite.

The research group found that filamentous fungi of the same species exhibit symbiotic nature in one strain and parasitic nature in another strain on the same plant. In addition, from the results of comparative transcriptome analysis of plant roots infected with one of the two strains, they found that only parasitic strains activate bacterial gene clusters that synthesize a secondary metabolite (a kind of terpenes) during infection, and that the activation is necessary for infection of the parasitic strain to the host roots and inhibition of plant growth. Furthermore, they found that the activation state of this gene cluster is affected by slight fluctuations in the surrounding temperature environment. They observed that when the temperature changed from 22°C to 26°C, the cluster activity disappeared, and the parasitic strain transformed into a symbiotic strain that promotes plant growth in an environment depleted of soluble phosphorus.
Finally, when the team created a bacterial mutant disrupted in the corresponding cluster of the parasitic strain and inoculated into plants, plant growth was improved to the same level as the symbiotic strain. These results suggest that the activation state of a single bacterial gene cluster changes with minute environmental fluctuations such as temperature changes in a day, and that such changes support the switching of contrasting directions from symbiosis to parasitism, and vice versa, in microorganisms. Interestingly, symbiotic strains, which also have this gene cluster, did not induce expression at all.

By further investigating the regulatory mechanism of this gene cluster and developing technologies to control cluster activation, this study is expected to lead to the development of technology to optimize the utility of symbiotic bacteria while suppressing only the detrimental behaviors of parasitic bacteria.

Original article
Nature Communications doi: 10.1038/s41467-023-40867-w
K. Hiruma, S. Aoki, J. Takino, T. Higa, Y. D. Utami, A. Shiina, M. Okamoto, M. Nakamura, N. Kawamura, Y. Ohmori, R. Sugita, K. Tanoi, T. Sato, H. Oikawa, A. Minami, W. Iwasaki, Y. Saijo,
"A fungal sesquiterpene biosynthesis gene cluster critical for mutualist-pathogen transition in Colletotrichum tofieldiae".
Contact
Masanori Okamoto
Team Leader
Plant Chemical Genetics Research Team