Display options
Cite
Ramundo S, Casero D, Mühlhaus T, et al. Conditional Depletion of the Chlamydomonas Chloroplast ClpP Protease Activates Nuclear Genes Involved in Autophagy and Plastid Protein Quality Control. Plant Cell. 2014;26(5):2201-2222doi: 10.1105/tpc.114.124842.
Ramundo, S., Casero, D., Mühlhaus, T., Hemme, D., Sommer, F., Crèvecoeur, M., Rahire, M., Schroda, M., Rusch, J., Goodenough, U., Pellegrini, M., Perez-Perez, M. E., Crespo, J. L., Schaad, O., Civic, N., & Rochaix, J. D. (2014). Conditional Depletion of the Chlamydomonas Chloroplast ClpP Protease Activates Nuclear Genes Involved in Autophagy and Plastid Protein Quality Control. The Plant cell, 26(5), 2201-2222. https://doi.org/10.1105/tpc.114.124842
Ramundo, Silvia, et al. "Conditional Depletion of the Chlamydomonas Chloroplast ClpP Protease Activates Nuclear Genes Involved in Autophagy and Plastid Protein Quality Control." The Plant cell vol. 26,5 (2014): 2201-2222. doi: https://doi.org/10.1105/tpc.114.124842
Ramundo S, Casero D, Mühlhaus T, Hemme D, Sommer F, Crèvecoeur M, Rahire M, Schroda M, Rusch J, Goodenough U, Pellegrini M, Perez-Perez ME, Crespo JL, Schaad O, Civic N, Rochaix JD. Conditional Depletion of the Chlamydomonas Chloroplast ClpP Protease Activates Nuclear Genes Involved in Autophagy and Plastid Protein Quality Control. Plant Cell. 2014 May;26(5):2201-2222. doi: 10.1105/tpc.114.124842. Epub 2014 May 30. PMID: 24879428; PMCID: PMC4079378.
Copy Download .nbib Format: NLM
Share it on

Plant Cell. 2014 May;26(5):2201-2222. doi: 10.1105/tpc.114.124842. Epub 2014 May 30.

Conditional Depletion of the Chlamydomonas Chloroplast ClpP Protease Activates Nuclear Genes Involved in Autophagy and Plastid Protein Quality Control.

The Plant cell

Silvia Ramundo, David Casero, Timo Mühlhaus, Dorothea Hemme, Frederik Sommer, Michèle Crèvecoeur, Michèle Rahire, Michael Schroda, Jannette Rusch, Ursula Goodenough, Matteo Pellegrini, Maria Esther Perez-Perez, José Luis Crespo, Olivier Schaad, Natacha Civic, Jean David Rochaix

Affiliations

  1. Departments of Molecular Biology and Plant Biology, University of Geneva, 1211 Geneva, Switzerland.
  2. Institute for Genomics and Proteomics, University of California, Los Angeles, California 90095.
  3. Max Planck Institute of Molecular Plant Physiology, D-14476 Potsdam-Golm Germany.
  4. Department of Biology, Washington University, St. Louis, Missouri 63130.
  5. Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, California 90095.
  6. Instituto de Bioquimica Vegetal y Fotosintesis, Consejo Superior de Investigaciones Cientificas, Universidad de Sevilla, 41092 Sevilla, Spain.
  7. Genomics Platform, University of Geneva, 1211 Geneva, Switzerland Department of Biochemistry, University of Geneva, 1211 Geneva, Switzerland.
  8. Genomics Platform, University of Geneva, 1211 Geneva, Switzerland.
  9. Departments of Molecular Biology and Plant Biology, University of Geneva, 1211 Geneva, Switzerland [email protected].

PMID: 24879428 PMCID: PMC4079378 DOI: 10.1105/tpc.114.124842

Abstract

Plastid protein homeostasis is critical during chloroplast biogenesis and responses to changes in environmental conditions. Proteases and molecular chaperones involved in plastid protein quality control are encoded by the nucleus except for the catalytic subunit of ClpP, an evolutionarily conserved serine protease. Unlike its Escherichia coli ortholog, this chloroplast protease is essential for cell viability. To study its function, we used a recently developed system of repressible chloroplast gene expression in the alga Chlamydomonas reinhardtii. Using this repressible system, we have shown that a selective gradual depletion of ClpP leads to alteration of chloroplast morphology, causes formation of vesicles, and induces extensive cytoplasmic vacuolization that is reminiscent of autophagy. Analysis of the transcriptome and proteome during ClpP depletion revealed a set of proteins that are more abundant at the protein level, but not at the RNA level. These proteins may comprise some of the ClpP substrates. Moreover, the specific increase in accumulation, both at the RNA and protein level, of small heat shock proteins, chaperones, proteases, and proteins involved in thylakoid maintenance upon perturbation of plastid protein homeostasis suggests the existence of a chloroplast-to-nucleus signaling pathway involved in organelle quality control. We suggest that this represents a chloroplast unfolded protein response that is conceptually similar to that observed in the endoplasmic reticulum and in mitochondria.

© 2014 American Society of Plant Biologists. All rights reserved.

References

  1. Plant J. 2006 Oct;48(1):1-16 - PubMed
  2. Plant Physiol. 2012 Aug;159(4):1428-39 - PubMed
  3. Plant Cell. 2012 Feb;24(2):637-59 - PubMed
  4. J Mol Biol. 2004 Oct 15;343(2):445-55 - PubMed
  5. Plant J. 2005 Feb;41(3):364-75 - PubMed
  6. FEBS J. 2005 Nov;272(21):5558-71 - PubMed
  7. J Proteome Res. 2013 Feb 1;12(2):547-58 - PubMed
  8. Plant Cell. 2011 Apr;23(4):1273-92 - PubMed
  9. Cell. 2005 May 20;121(4):529-539 - PubMed
  10. Eukaryot Cell. 2009 Dec;8(12):1856-68 - PubMed
  11. Autophagy. 2012 Mar;8(3):376-88 - PubMed
  12. Plant Cell. 2006 Jul;18(7):1704-21 - PubMed
  13. Biochim Biophys Acta. 2011 Aug;1807(8):999-1011 - PubMed
  14. Curr Genet. 2002 Aug;41(5):291-310 - PubMed
  15. Nat Struct Biol. 2001 Mar;8(3):230-3 - PubMed
  16. Mol Cell. 2002 Mar;9(3):673-83 - PubMed
  17. Cell. 1993 Jun 18;73(6):1197-206 - PubMed
  18. Cell. 2007 Dec 14;131(6):1137-48 - PubMed
  19. J Biol Chem. 2009 Jun 5;284(23):15408-15 - PubMed
  20. Proc Natl Acad Sci U S A. 1965 Dec;54(6):1665-9 - PubMed
  21. Nat Cell Biol. 2005 Dec;7(12):1224-31 - PubMed
  22. Plant Cell. 2013 Jan;25(1):167-86 - PubMed
  23. J Cell Sci. 2011 Feb 1;124(Pt 3):469-82 - PubMed
  24. Science. 1991 Nov 29;254(5036):1374-7 - PubMed
  25. Nature. 1999 Sep 2;401(6748):90-3 - PubMed
  26. Mol Gen Genet. 1994 Jul 25;244(2):151-9 - PubMed
  27. Mol Cell. 2010 Nov 12;40(3):465-80 - PubMed
  28. Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7463-8 - PubMed
  29. J Biol Chem. 1996 Sep 6;271(36):21848-52 - PubMed
  30. Planta. 2000 May;210(6):897-905 - PubMed
  31. Plant Signal Behav. 2013 Mar;8(3):e23198 - PubMed
  32. Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):4238-42 - PubMed
  33. Mol Microbiol. 2006 May;60(3):723-37 - PubMed
  34. Nat Cell Biol. 2012 Feb 02;14(2):117-23 - PubMed
  35. J Biol Chem. 2001 Jun 1;276(22):18843-8 - PubMed
  36. Nature. 2003 Sep 4;425(6953):86-9 - PubMed
  37. Mol Cell Proteomics. 2011 Sep;10(9):M110.004739 - PubMed
  38. Plant Cell. 2006 Jun;18(6):1454-66 - PubMed
  39. Cold Spring Harb Symp Quant Biol. 2006;71:505-11 - PubMed
  40. Physiol Plant. 2012 May;145(1):224-34 - PubMed
  41. Plant Physiol. 2005 Dec;139(4):1736-49 - PubMed
  42. BMC Bioinformatics. 2011 Jul 12;12:282 - PubMed
  43. Nat Rev Mol Cell Biol. 2009 Jul;10(7):458-67 - PubMed
  44. Mol Biol Cell. 2005 Mar;16(3):1165-77 - PubMed
  45. Methods Mol Biol. 2008;445:29-76 - PubMed
  46. PLoS One. 2007 Sep 12;2(9):e874 - PubMed
  47. Plant Cell. 2000 Jan;12(1):137-50 - PubMed
  48. Mol Cell Proteomics. 2009 Aug;8(8):1789-1810 - PubMed
  49. Plant Mol Biol. 2012 Sep;80(2):189-202 - PubMed
  50. Plant Physiol. 2001 Apr;125(4):1912-8 - PubMed
  51. Mol Biol Evol. 2012 Dec;29(12):3625-39 - PubMed
  52. Curr Opin Plant Biol. 2006 Jun;9(3):234-40 - PubMed
  53. Plant Cell. 2011 Jan;23(1):322-32 - PubMed
  54. EMBO Rep. 2009 May;10(5):508-14 - PubMed
  55. Plant Mol Biol. 2007 Jan;63(1):85-96 - PubMed
  56. Plant Signal Behav. 2007 May;2(3):185-7 - PubMed
  57. Prog Lipid Res. 2011 Apr;50(2):141-51 - PubMed
  58. Plant Physiol. 2010 Apr;152(4):1874-88 - PubMed
  59. Genome Biol. 2010;11(10):R106 - PubMed
  60. Arch Microbiol. 2005 Jan;183(1):66-9 - PubMed
  61. Plant Cell. 2009 Jun;21(6):1669-92 - PubMed
  62. J Biol Chem. 2001 Sep 7;276(36):33645-51 - PubMed
  63. Eukaryot Cell. 2014 May;13(5):591-613 - PubMed
  64. Cell. 2011 Jul 22;146(2):290-302 - PubMed
  65. Photosynth Res. 1996 Mar;47(3):267-80 - PubMed
  66. Bioinformatics. 2014 Jan 15;30(2):197-205 - PubMed
  67. Cell. 2007 Jun 15;129(6):1189-200 - PubMed
  68. Curr Biol. 2011 Sep 27;21(18):R697-9 - PubMed
  69. Plant Cell Physiol. 2001 Mar;42(3):264-73 - PubMed
  70. Bioinformatics. 2013 Jan 1;29(1):15-21 - PubMed
  71. Nat Biotechnol. 2008 Mar;26(3):317-25 - PubMed
  72. Mol Cell. 2003 Mar;11(3):671-83 - PubMed
  73. Cell. 1997 Nov 14;91(4):447-56 - PubMed
  74. Plant Cell. 2006 Oct;18(10):2635-49 - PubMed
  75. EMBO J. 1997 Feb 3;16(3):659-71 - PubMed
  76. J Struct Biol. 2006 Feb;153(2):113-28 - PubMed
  77. Nat Cell Biol. 2007 Oct;9(10):1102-9 - PubMed
  78. Proc Natl Acad Sci U S A. 2007 Dec 26;104(52):20770-5 - PubMed
  79. Proc Natl Acad Sci U S A. 2007 Apr 3;104(14):5883-8 - PubMed
  80. Trends Plant Sci. 2002 Oct;7(10):451-6 - PubMed
  81. J Electron Microsc (Tokyo). 2011;60 Suppl 1:S3-29 - PubMed
  82. Biochim Biophys Acta. 2013 Dec;1828(12):2933-6 - PubMed
  83. Microbiology (Reading). 2002 Jul;148(Pt 7):2255-2265 - PubMed
  84. Nat Struct Mol Biol. 2006 Nov;13(11):1002-9 - PubMed
  85. Curr Genet. 2008 Jun;53(6):381-8 - PubMed
  86. Autophagy. 2008 Oct;4(7):851-65 - PubMed
  87. J Biol Chem. 2004 Feb 6;279(6):4768-81 - PubMed

Publication Types

Grant support