Department of Chemistry and Biochemistry, University of California San Diego, La Jolla, United States; Department of Developmental and Cell Biology and Center for Complex Biological Systems, University of California Irvine, Irvine, United States; Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Japan
Matheus P Viana
Department of Developmental and Cell Biology and Center for Complex Biological Systems, University of California Irvine, Irvine, United States
Fan Xu
Department of Chemistry and Biochemistry, University of California San Diego, La Jolla, United States
Jingwen Yu
Department of Chemistry and Biochemistry, University of California San Diego, La Jolla, United States
Raghav Chanchani
Department of Chemistry and Biochemistry, University of California San Diego, La Jolla, United States
Ximena G Arceo
Department of Chemistry and Biochemistry, University of California San Diego, La Jolla, United States
Department of Anatomy and Structural Biology, Albert Einstein College of Medicine, Bronx, United States; Gruss-Lipper Biophotonics Center, Albert Einstein College of Medicine, Bronx, United States; Department of Neuroscience, Albert Einstein College of Medicine, Bronx, United States; Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
Susanne M Rafelski
Department of Developmental and Cell Biology and Center for Complex Biological Systems, University of California Irvine, Irvine, United States
Mitochondria are dynamic organelles that must precisely control their protein composition according to cellular energy demand. Although nuclear-encoded mRNAs can be localized to the mitochondrial surface, the importance of this localization is unclear. As yeast switch to respiratory metabolism, there is an increase in the fraction of the cytoplasm that is mitochondrial. Our data point to this change in mitochondrial volume fraction increasing the localization of certain nuclear-encoded mRNAs to the surface of the mitochondria. We show that mitochondrial mRNA localization is necessary and sufficient to increase protein production to levels required during respiratory growth. Furthermore, we find that ribosome stalling impacts mRNA sensitivity to mitochondrial volume fraction and counterintuitively leads to enhanced protein synthesis by increasing mRNA localization to mitochondria. This points to a mechanism by which cells are able to use translation elongation and the geometric constraints of the cell to fine-tune organelle-specific gene expression through mRNA localization.