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

Author

Listed:
  • Josep Vilarrasa-Blasi

    (Stanford University
    Carnegie Institution for Science, Department of Plant Biology)

  • Tamara Vellosillo

    (Stanford University
    Carnegie Institution for Science, Department of Plant Biology)

  • Robert E. Jinkerson

    (Carnegie Institution for Science, Department of Plant Biology
    University of California Riverside)

  • Friedrich Fauser

    (Carnegie Institution for Science, Department of Plant Biology
    Princeton University)

  • Tingting Xiang

    (Carnegie Institution for Science, Department of Plant Biology
    University of North Carolina at Charlotte)

  • 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
    Princeton University)

  • José R. Dinneny

    (Stanford University
    Carnegie Institution for Science, Department of Plant Biology)

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.

Suggested Citation

  • Josep Vilarrasa-Blasi & Tamara Vellosillo & Robert E. Jinkerson & Friedrich Fauser & Tingting Xiang & Benjamin B. Minkoff & Lianyong Wang & Kiril Kniazev & Michael Guzman & Jacqueline Osaki & Gregory , 2024. "Multi-omics analysis of green lineage osmotic stress pathways unveils crucial roles of different cellular compartments," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49844-3
    DOI: 10.1038/s41467-024-49844-3
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    References listed on IDEAS

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    1. Gal Masrati & Manish Dwivedi & Abraham Rimon & Yael Gluck-Margolin & Amit Kessel & Haim Ashkenazy & Itay Mayrose & Etana Padan & Nir Ben-Tal, 2018. "Broad phylogenetic analysis of cation/proton antiporters reveals transport determinants," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    2. Fang Yuan & Huimin Yang & Yan Xue & Dongdong Kong & Rui Ye & Chijun Li & Jingyuan Zhang & Lynn Theprungsirikul & Tayler Shrift & Bryan Krichilsky & Douglas M. Johnson & Gary B. Swift & Yikun He & Jame, 2014. "OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis," Nature, Nature, vol. 514(7522), pages 367-371, October.
    3. Yohei Takahashi & Jingbo Zhang & Po-Kai Hsu & Paulo H. O. Ceciliato & Li Zhang & Guillaume Dubeaux & Shintaro Munemasa & Chennan Ge & Yunde Zhao & Felix Hauser & Julian I. Schroeder, 2020. "MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
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