Modulation of fungal phosphate homeostasis by the plant hormone strigolactone.

Shelley Lumba, Yuichiro Tsuchiya, Christopher S P McErlean, Nina Marsh, Omar As'sadiq, Dylan Bradizza, Shingo Suginoo, Duncan Holbrook-Smith, Flora Zhiqi Wang, George Ly, Naoki Kato, James M Bradley, Bruno Aquino, Rajagopal Subramaniam, Hiroyuki Osada, Peter McCourt, Michael Bunsick, François-Didier Boyer, Dario Bonetta

Journal: Molecular cell 2024;84(20):4031-4047.e11

PMID: 39357514

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Abstract

Inter-kingdom communication through small molecules is essential to the coexistence of organisms in an ecosystem. In soil communities, the plant root is a nexus of interactions for a remarkable number of fungi and is a source of small-molecule plant hormones that shape fungal compositions. Although hormone signaling pathways are established in plants, how fungi perceive and respond to molecules is unclear because many plant-associated fungi are recalcitrant to experimentation. Here, we develop an approach using the model fungus, Saccharomyces cerevisiae, to elucidate mechanisms of fungal response to plant hormones. Two plant hormones, strigolactone and methyl jasmonate, produce unique transcript profiles in yeast, affecting phosphate and sugar metabolism, respectively. Genetic analysis in combination with structural studies suggests that SLs require the high-affinity transporter Pho84 to modulate phosphate homeostasis. The ability to study small-molecule plant hormones in a tractable genetic system should have utility in understanding fungal-plant interactions.

Address: Department of Cell & Systems Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada.; Institute of Molecular Systems Biology, ETH, Zurich, Switzerland.; Department of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa, Nagoya 464-8601, Japan.; RIKEN Center for Sustainable Research Science, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan.; Université Paris-Saclay, CNRS, Institut de Chimie des Substances Naturelles, UPR 2301, 91198 Gif-sur-Yvette, France.; School of Chemistry, The University of Sydney, Sydney, NSW 2006, Australia.; Institute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan.; Agriculture and Agri-Food Canada, Ottawa, ON, Canada.; Ontario Tech University, 2000 Simcoe St. N, Oshawa, ON L1G 0C5, Canada.; Department of Cell & Systems Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada; Centre for the Analysis of Genome Evolution and Function, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada. Electronic address: [email protected].; Department of Cell & Systems Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada; Centre for the Analysis of Genome Evolution and Function, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada. Electronic address: [email protected].

DOI: 10.1016/j.molcel.2024.09.004

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MeSH Terms: Lactones, Phosphates, Plant Growth Regulators, Homeostasis, Saccharomyces cerevisiae, Oxylipins, Cyclopentanes, Heterocyclic Compounds, 3-Ring, Acetates, Saccharomyces cerevisiae Proteins, Gene Expression Regulation, Fungal, Signal Transduction, Models, Molecular, Proton-Phosphate Symporters