Multi-omics analysis of green lineage osmotic stress pathways unveils crucial roles of different cellular compartments

Josep Vilarrasa-Blasi (), Tamara Vellosillo, Robert E. Jinkerson, Friedrich Fauser, Tingting Xiang, Benjamin B. Minkoff, Lianyong Wang, Kiril Kniazev, Michael Guzman, Jacqueline Osaki, Gregory A. Barrett-Wilt, Michael R. Sussman, Martin C. Jonikas and José R. Dinneny ()
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Josep Vilarrasa-Blasi: Stanford University
Tamara Vellosillo: Stanford University
Robert E. Jinkerson: Carnegie Institution for Science, Department of Plant Biology
Friedrich Fauser: Carnegie Institution for Science, Department of Plant Biology
Tingting Xiang: Carnegie Institution for Science, Department of Plant Biology
Benjamin B. Minkoff: University of Wisconsin
Lianyong Wang: Princeton University
Kiril Kniazev: Stanford University
Michael Guzman: Carnegie Institution for Science, Department of Plant Biology
Jacqueline Osaki: Carnegie Institution for Science, Department of Plant Biology
Gregory A. Barrett-Wilt: University of Wisconsin
Michael R. Sussman: University of Wisconsin
Martin C. Jonikas: Carnegie Institution for Science, Department of Plant Biology
José R. Dinneny: Stanford University

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Maintenance of water homeostasis is a fundamental cellular process required by all living organisms. Here, we use the single-celled green alga Chlamydomonas reinhardtii to establish a foundational understanding of osmotic-stress signaling pathways through transcriptomics, phosphoproteomics, and functional genomics approaches. Comparison of pathways identified through these analyses with yeast and Arabidopsis allows us to infer their evolutionary conservation and divergence across these lineages. 76 genes, acting across diverse cellular compartments, were found to be important for osmotic-stress tolerance in Chlamydomonas through their functions in cytoskeletal organization, potassium transport, vesicle trafficking, mitogen-activated protein kinase and chloroplast signaling. We show that homologs for five of these genes have conserved functions in stress tolerance in Arabidopsis and reveal a novel PROFILIN-dependent stage of acclimation affecting the actin cytoskeleton that ensures tissue integrity upon osmotic stress. This study highlights the conservation of the stress response in algae and land plants, and establishes Chlamydomonas as a unicellular plant model system to dissect the osmotic stress signaling pathway.

Date: 2024
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DOI: 10.1038/s41467-024-49844-3

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