A fungal sesquiterpene biosynthesis gene cluster critical for mutualist-pathogen transition in Colletotrichum tofieldiae

Kei Hiruma (), Seishiro Aoki, Junya Takino, Takeshi Higa, Yuniar Devi Utami, Akito Shiina, Masanori Okamoto, Masami Nakamura, Nanami Kawamura, Yoshihiro Ohmori, Ryohei Sugita, Keitaro Tanoi, Toyozo Sato, Hideaki Oikawa, Atsushi Minami, Wataru Iwasaki and Yusuke Saijo
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Kei Hiruma: The University of Tokyo
Seishiro Aoki: The University of Tokyo
Junya Takino: Hokkaido University
Takeshi Higa: The University of Tokyo
Yuniar Devi Utami: The University of Tokyo
Akito Shiina: The University of Tokyo
Masanori Okamoto: Utsunomiya University
Masami Nakamura: The University of Tokyo
Nanami Kawamura: Nara Institute of Science and Technology
Yoshihiro Ohmori: The University of Tokyo
Ryohei Sugita: Nagoya University
Keitaro Tanoi: The University of Tokyo
Toyozo Sato: National Agriculture and Food Research Organization
Hideaki Oikawa: Wuyi University
Atsushi Minami: Hokkaido University
Wataru Iwasaki: The University of Tokyo
Yusuke Saijo: Nara Institute of Science and Technology

Nature Communications, 2023, vol. 14, issue 1, 1-18

Abstract: Abstract Plant-associated fungi show diverse lifestyles from pathogenic to mutualistic to the host; however, the principles and mechanisms through which they shift the lifestyles require elucidation. The root fungus Colletotrichum tofieldiae (Ct) promotes Arabidopsis thaliana growth under phosphate limiting conditions. Here we describe a Ct strain, designated Ct3, that severely inhibits plant growth. Ct3 pathogenesis occurs through activation of host abscisic acid pathways via a fungal secondary metabolism gene cluster related to the biosynthesis of sesquiterpene metabolites, including botrydial. Cluster activation during root infection suppresses host nutrient uptake-related genes and changes mineral contents, suggesting a role in manipulating host nutrition state. Conversely, disruption or environmental suppression of the cluster renders Ct3 beneficial for plant growth, in a manner dependent on host phosphate starvation response regulators. Our findings indicate that a fungal metabolism cluster provides a means by which infectious fungi modulate lifestyles along the parasitic–mutualistic continuum in fluctuating environments.

Date: 2023
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DOI: 10.1038/s41467-023-40867-w

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