Identification of green lineage osmotic stress pathways uncovers a role for actin during stress acclimation

Abstract

Maintenance of water homeostasis is a fundamental cellular process required by all living organisms. Here, we use the green alga Chlamydomonas reinhardtii to establish a foundational understanding of evolutionarily conserved osmotic-stress signaling pathways in the green lineage through transcriptomics, phosphoproteomics, and functional genomics approaches. Five genes acting across diverse cellular pathways were found to be essential for osmotic-stress tolerance in Chlamydomonas including cytoskeletal organization, potassium transport, vesicle trafficking, mitogen-activated protein kinase and chloroplast signaling. We show that homologs of these genes in the multicellular land plant Arabidopsis thaliana have conserved functional roles in stress tolerance and reveal a novel PROFILIN-dependent actin remodeling stage of acclimation that ensures cell survival and 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.