Exploring MARS: an investigation of mutants affected in chloroplast-to-nucleus retrograde signaling
Karina Perlaza1, Hannah Toutkoushian1, Mable Lam1, Morgane Boone1, Martin Jonikas2, Peter Walter1, Silvia Ramundo1 1Department of Biochemistry and Biophysics, University of California, San Francisco 2Department of Molecular Biology, Princeton University, New Jersey
Chloroplasts are specialized compartments in plant cells responsible for harvesting light energy via photosynthesis. Chloroplasts have retained their own protein-encoding genome, even after billions of years of evolution from their cyanobacterial origins. This leads to an important challenge for eukaryotic photosynthetic organisms: the necessity to coordinate nuclear and chloroplast gene expression so to maintain homeostasis in response to environmental stressors and variable cellular needs. Proteotoxic stress in the chloroplast, induced by inactivation of the ClpP1 protease which normally degrades misfolded chloroplast proteins, triggers a massive increase in the expression of nuclear-encoded, chloroplast-localized chaperones and proteases, as well as proteins involved in chloroplast membrane biogenesis. Remarkably, most of these genes are also transcriptionally upregulated during exposure to higher than normal light intensity (HL), another condition that causes a protein homeostatic imbalance in the chloroplast. These results reveal the existence of a chloroplast unfolded protein response (cpUPR), an organelle quality control pathway that is analogous to the signaling pathways observed in response to endoplasmic reticulum or mitochondrial stress. To identify factors that mediate the cpUPR, we carried out a forward genetic screen in Chlamydomonas reinhardtii that yielded mutants affected in chloroplast-to-nucleus retrograde signaling (MARS). We identified two mutants that were defective in inducing cpUPR signaling upon ClpP1 inactivation and HL stress. Each carries a different mutant allele of a previously uncharacterized gene encoding a serine kinase, herein referred to as MARS1. We show that the Mars1 kinase activity is required for cpUPR signaling upon chloroplast stress. Moreover, mars1 mutants exhibit increased sensitivity to HL, thus emphasizing the physiological importance of this pathway. Our results underscore the importance of retrograde signaling in response to chloroplast stress, and establish MARS1 as the first gene identified in this novel cpUPR signaling pathway.
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