- Published Version
Official URL: http://dx.doi.org/10.1083/jcb.200805125
Eukaryotic cells under stress repress translation and localize these messenger RNAs (mRNAs) to cytoplasmic RNA granules. We show that specific stress stimuli induce the assembly of RNA granules in an organelle with bacterial ancestry, the chloroplast of Chlamydomonas reinhardtii. These chloroplast stress granules (cpSGs) form during oxidative stress and disassemble during recovery from stress. Like mammalian stress granules, cpSGs contain poly(A)-binding protein and the small, but not the large, ribosomal subunit. In addition, mRNAs are in continuous flux between polysomes and cpSGs during stress. Localization of cpSGs within the pyrenoid reveals that this chloroplast compartment functions in this stress response. The large subunit of ribulosebisphosphate carboxylase/oxygenase also assembles into cpSGs and is known to bind mRNAs during oxidative stress, raising the possibility that it plays a role in cpSG assembly. This discovery within such an organelle suggests that mRNA localization to granules during stress is a more general phenomenon than currently realized.
|Divisions:||Concordia University > Faculty of Arts and Science > Biology|
|Authors:||Uniacke, James and Zerges, William|
|Journal or Publication:||Journal of Cell Biology|
|Date:||18 August 2008|
|Deposited By:||DANIELLE DENNIE|
|Deposited On:||16 May 2011 15:35|
|Last Modified:||24 Aug 2016 21:26|
Adir, N., S. Shochat, and I. Ohad. 1990. Light-dependent D1 protein synthesis and translocation is regulated by reaction center II. Reaction center II serves as an acceptor for the D1 precursor. J. Biol. Chem. 265:12563–12568.
Anderson, P., and N. Kedersha. 2008. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33:141–150.
Beligni, M.V., K. Yamaguchi, and S.P. Mayfield. 2004. The translational apparatus of Chlamydomonas reinhardtii chloroplast. Photosynth. Res. 82:315–325.
Cohen, I., Y. Sapir, and M. Shapira. 2006. A conserved mechanism controls translation of Rubisco large subunit in different photosynthetic organisms. Plant Physiol. 141:1089–1097.
Colon-Ramos, D.A., J.L. Salisbury, M.A. Sanders, S.M. Shenoy, R.H. Singer, and M.A. Garcia-Blanco. 2003. Asymmetric distribution of nuclear pore complexes and the cytoplasmic localization of beta2-tubulin mRNA in Chlamydomonas reinhardtii. Dev. Cell. 4:941–952.
Fischer, B.B., A. Krieger-Liszkay, and R.L. Eggen. 2004. Photosensitizers neutral red (type I) and rose bengal (type II) cause light-dependent toxicity in Chlamydomonas reinhardtii and induce the Gpxh gene via increased singlet oxygen formation. Environ. Sci. Technol. 38:6307–6313.
Hideg, E., P.B. Kos, and I. Vass. 2007. Photosystem II damage induced by chemically generated singlet oxygen in tobacco leaves. Physiol. Plant. 131:33–40.
Hoffmann, X.K., and C.F. Beck. 2005. Mating-induced shedding of cell walls, removal of walls from vegetative cells, and osmotic stress induce presumed cell wall genes in Chlamydomonas. Plant Physiol. 139:999–1014.
Kedersha, N., and P. Anderson. 2002. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30:963–969.
Kedersha, N., M.R. Cho, W. Li, P.W. Yacono, S. Chen, N. Gilks, D.E. Golan, and P. Anderson. 2000. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151:1257–1268.
Kedersha, N., G. Stoecklin, M. Ayodele, P. Yacono, J. Lykke-Andersen, M.J. Fritzler, D. Scheuner, R.J. Kaufman, D.E. Golan, and P. Anderson. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169:871–884.
Knopf, J.A., and M. Shapira. 2005. Degradation of Rubisco SSU during oxidative stress triggers aggregation of Rubisco particles in Chlamydomonas reinhardtii. Planta. 222:787–793.
Liu, C., F. Willmund, J.P. Whitelegge, S. Hawat, B. Knapp, M. Lodha, and M. Schroda. 2005. J-domain protein CDJ2 and HSP70B are a plastidic chaperone pair that interacts with vesicle-inducing protein in plastids 1. Mol. Biol. Cell. 16:1165–1177.
Mazroui, R., R. Sukarieh, M.E. Bordeleau, R.J. Kaufman, P. Northcote, J. Tanaka, I. Gallouzi, and J. Pelletier. 2006. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol. Biol. Cell. 17:4212–4219.
Michael, R., L. McKay, and S.P. Gibbs. 1991. Composition and function of pyrenoids: cytochemical and immunocytochemical approaches. Can. J. Bot. 69:1040–1052.
Moseley, J.L., C.W. Chang, and A.R. Grossman. 2006. Genome-based approaches to understanding phosphorus deprivation responses and PSR1 control in Chlamydomonas reinhardtii. Eukaryot. Cell. 5:26–44.
Murata, N., S. Takahashi, Y. Nishiyama, and S.I. Allakhverdiev. 2007. Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta. 1767:414–421.
Nishiyama, Y., S.I. Allakhverdiev, and N. Murata. 2006. A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim. Biophys. Acta. 1757:742–749.
Nover, L., K.D. Scharf, and D. Neumann. 1989. Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol. Cell. Biol. 9:1298–1308.
Ohad, I., P. Siekevitz, and G.E. Palade. 1967. Biogenesis of chloroplast membranes. II. Plastid differentiation during greening of a dark-grown algal mutant (Chlamydomonas reinhardi). J. Cell Biol. 35:553–584.
Parker, R., and U. Sheth. 2007. P bodies and the control of mRNA translation and degradation. Mol. Cell. 25:635–646.
Stohr, N., M. Lederer, C. Reinke, S. Meyer, M. Hatzfeld, R.H. Singer, and S. Huttelmaier. 2006. ZBP1 regulates mRNA stability during cellular stress. J. Cell Biol. 175:527–534.
Sueoka, N. 1960. Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardi. Proc. Natl. Acad. Sci. USA. 46:83–91.
Suss, K.H., I. Prokhorenko, and K. Adler. 1995. In situ association of Calvin cycle enzymes, ribulose-1,5-bisphosphate carboxylase/oxygenase activase, ferredoxin-NADP+ reductase, and nitrite reductase with thylakoid and pyrenoid membranes of Chlamydomonas reinhardtii chloroplasts as revealed by immunoelectron microscopy. Plant Physiol. 107:1387–1397.
Trebitsh, T., A. Levitan, A. Sofer, and A. Danon. 2000. Translation of chloroplast psbA mRNA is modulated in the light by counteracting oxidizing and reducing activities. Mol. Cell. Biol. 20:1116–1123.
Uniacke, J., and W. Zerges. 2007. Photosystem II assembly and repair are differentially localized in Chlamydomonas. Plant Cell. 19:3640–3654.
von Gromoff, E.D., U. Treier, and C.F. Beck. 1989. Three light-inducible heat shock genes of Chlamydomonas reinhardtii. Mol. Cell. Biol. 9:3911–3918.
Yohn, C.B., A. Cohen, A. Danon, and S.P. Mayfield. 1998. A poly(A) binding protein functions in the chloroplast as a message-specific translation factor. Proc. Natl. Acad. Sci. USA. 95:2238–2243.
Yosef, I., V. Irihimovitch, J.A. Knopf, I. Cohen, I. Orr-Dahan, E. Nahum, C. Keasar, and M. Shapira. 2004. RNA binding activity of the ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit from Chlamydomonas reinhardtii. J. Biol. Chem. 279:10148–10156.
Repository Staff Only: item control page