Abstract
Plastids (including chloroplasts) are subcellular sites for a plethora of proteolytic reactions, required in functions ranging from protein biogenesis to quality control. Here we show that peptides generated from pre-protein maturation within chloroplasts of Arabidopsis thaliana are degraded to amino acids by a multi-step peptidolytic cascade consisting of oligopeptidases and aminopeptidases, effectively allowing the recovery of single amino acids within these organelles.
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References
Zimorski, V., Ku, C., Martin, W.F. & Gould, S.B. Curr. Opin. Microbiol. 22, 38–48 (2014).
Schleiff, E. & Becker, T. Nat. Rev. Mol. Cell Biol. 12, 48–59 (2011).
Teixeira, P.F. & Glaser, E. Biochim. Biophys. Acta 1833, 360–370 (2013).
Kmiec, B., Teixeira, P.F. & Glaser, E. Trends Plant Sci. 19, 771–778 (2014).
Johnson, K.A. et al. EMBO J. 25, 1977–1986 (2006).
Kmiec, B. et al. Proc. Natl. Acad. Sci. USA 110, E3761–E3769 (2013).
Stahl, A. et al. J. Biol. Chem. 277, 41931–41939 (2002).
Bhushan, S. et al. EMBO Rep. 4, 1073–1078 (2003).
Lowther, W.T. & Matthews, B.W. Chem. Rev. 102, 4581–4608 (2002).
Beninga, J., Rock, K.L. & Goldberg, A.L. J. Biol. Chem. 273, 18734–18742 (1998).
Kelly, J.A., Neidle, E.L. & Neidle, A. J. Neurochem. 40, 1727–1734 (1983).
Stoltze, L. et al. Nat. Immunol. 1, 413–418 (2000).
Walling, L.L. Curr. Opin. Plant Biol. 9, 227–233 (2006).
van Wijk, K.J. Annu. Rev. Plant Biol. 66, 75–111 (2015).
Ferro, M. et al. Mol. Cell. Proteomics 9, 1063–1084 (2010).
Kleffmann, T. et al. Curr. Biol. 14, 354–362 (2004).
Narváez-Vásquez, J., Tu, C.J., Park, S.Y. & Walling, L.L. Planta 227, 341–351 (2008).
Rowland, E., Kim, J., Bhuiyan, N.H. & van Wijk, K.J. Plant Physiol. 169, 1881–1896 (2015).
Law, S.R. et al. Plant Physiol. 158, 1610–1627 (2012).
Bhushan, S., Kuhn, C., Berglund, A.K., Roth, C. & Glaser, E. FEBS Lett. 580, 3966–3972 (2006).
Polge, C. et al. J. Biol. Chem. 284, 35412–35424 (2009).
Saric, T., Graef, C.I. & Goldberg, A.L. J. Biol. Chem. 279, 46723–46732 (2004).
Vabulas, R.M. & Hartl, F.U. Science 310, 1960–1963 (2005).
Carrie, C. et al. Plant J. 57, 1128–1139 (2009).
Aronsson, H. & Jarvis, P. FEBS Lett. 529, 215–220 (2002).
Hall, M., Mishra, Y. & Schröder, W.P. Methods Mol. Biol. 775, 207–222 (2011).
Murcha, M.W., Elhafez, D., Millar, A.H. & Whelan, J. J. Biol. Chem. 280, 16476–16483 (2005).
Teixeira, P.F., Branca, R.M., Kmiec, B. & Glaser, E. Methods Mol. Biol. 1305, 123–130 (2015).
Zybailov, B. et al. PLoS One 3, e1994 (2008).
Drag, M., Bogyo, M., Ellman, J.A. & Salvesen, G.S. J. Biol. Chem. 285, 3310–3318 (2010).
Kmiec, B., Teixeira, P.F. & Glaser, E. Biochimie 100, 167–170 (2014).
Acknowledgements
We would like to thank the Swedish Metabolomics Centre (Umeå) for assistance with amino acid quantification, H. Fu (Academia Sinica) for Rpn10 antisera and U. Langel (Stockholm University) for the galanin peptide. This study was supported by grants from the Swedish Research Council to E.G. (DN2015-04833) and J.L. (DN2012-5145), from the Sigurd och Elsa Goljes Minne Foundation to P.F.T. and B.K., the ARC future fellowship to M.W.M., ARC Discovery program grant DP130102384 to J.W., Polish National Science Centre for Scientific Research grant NN401042838 to M.D. and the STINT Institutional grant for cooperation between the laboratories of E.G. and J.W.
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P.F.T. designed the study and performed peptidase assays. B.K. selected and characterized Arabidopsis mutants and performed cellular fractionation experiments. R.M.M.B. carried out peptide MS analysis. M.W.M. performed protein localization experiments. A.B. carried out aminopeptidase profiling. P.F.T., B.K., R.M.M.B., A.B., M.W.M., A.I., J.W., M.D., J.L. and E.G. analyzed, discussed and interpreted the results. P.F.T. and B.K. wrote the paper with input from all coauthors.
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Supplementary Results, Supplementary Figures 1–7 and Supplementary Tables 1–4. (PDF 1906 kb)
Supplementary Data Set 1
Original mass spectrometry data. (XLSX 56 kb)
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Teixeira, P., Kmiec, B., Branca, R. et al. A multi-step peptidolytic cascade for amino acid recovery in chloroplasts. Nat Chem Biol 13, 15–17 (2017). https://doi.org/10.1038/nchembio.2227
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DOI: https://doi.org/10.1038/nchembio.2227
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