First published online November 24, 2004; 10.1104/pp.104.053835
Plant Physiology 136:4114-4126 (2004)
© 2004 American Society of Plant Biologists
CELL BIOLOGY AND SIGNAL TRANSDUCTION
Inactivation of the clpC1 Gene Encoding a Chloroplast Hsp100 Molecular Chaperone Causes Growth Retardation, Leaf Chlorosis, Lower Photosynthetic Activity, and a Specific Reduction in Photosystem Content1
Lars L.E. Sjögren,
Tara M. MacDonald,
Sirkka Sutinen and
Adrian K. Clarke*
Botanical Institute, Göteborg University, SE405 30 Göteborg, Sweden (L.L.E.S., T.M.M., A.K.C.); and The Finnish Forest Research Institute, Joensuu Research Center, Fin801 01, Finland (S.S.)
ClpC is a molecular chaperone of the Hsp100 family. In higher plants there are two chloroplast-localized paralogs (ClpC1 and ClpC2) that are approximately 93% similar in primary sequence. In this study, we have characterized two independent Arabidopsis (Arabidopsis thaliana) clpC1 T-DNA insertion mutants lacking on average 65% of total ClpC content. Both mutants display a retarded-growth phenotype, leaves with a homogenous chlorotic appearance throughout all developmental stages, and more perpendicular secondary influorescences. Photosynthetic performance was also impaired in both knockout lines, with relatively fewer photosystem I and photosystem II complexes, but no changes in ATPase and Rubisco content. However, despite the specific drop in photosystem I and photosystem II content, no changes in leaf cell anatomy or chloroplast ultrastructure were observed in the mutants compared to the wild type. Previously proposed functions for envelope-associated ClpC in chloroplast protein import and degradation of mistargeted precursors were examined and shown not to be significantly impaired in the clpC1 mutants. In the stroma, where the majority of ClpC protein is localized, marked increases of all ClpP paralogs were observed in the clpC1 mutants but less variation for the ClpR paralogs and a corresponding decrease in the other chloroplast-localized Hsp100 protein, ClpD. Increased amounts of other stromal molecular chaperones (Cpn60, Hsp70, and Hsp90) and several RNA-binding proteins were also observed. Our data suggest that overall ClpC as a stromal molecular chaperone plays a vital role in chloroplast function and leaf development and is likely involved in photosystem biogenesis.
1 This work was supported by the Swedish Research Council (VR), the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas), the Swedish Foundation for International Cooperation in Research and Education (STINT), and an overseas postgraduate scholarship from the Natural Sciences and Engineering Research Council of Canada (to T.M.M.).
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.053835.
* Corresponding author; e-mail adrian.clarke{at}botany.gu.se; fax 46317732626.
Received September 21, 2004;
returned for revision October 7, 2004;
accepted October 9, 2004.
This article has been cited by other articles:

|
 |

|
 |
 
P. Boij, R. Patel, C. Garcia, P. Jarvis, and H. Aronsson
In vivo Studies on the Roles of Tic55-Related Proteins in Chloroplast Protein Import in Arabidopsis thaliana
Mol Plant,
October 11, 2009;
(2009)
ssp079v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Ogawa, K. Nishimura, T. Aoki, H. Takase, K.-I. Tomizawa, H. Ashida, and A. Yokota
A Phosphofructokinase B-Type Carbohydrate Kinase Family Protein, NARA5, for Massive Expressions of Plastid-Encoded Photosynthetic Genes in Arabidopsis
Plant Physiology,
September 1, 2009;
151(1):
114 - 128.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Zybailov, G. Friso, J. Kim, A. Rudella, V. R. Rodriguez, Y. Asakura, Q. Sun, and K. J. van Wijk
Large Scale Comparative Proteomics of a Chloroplast Clp Protease Mutant Reveals Folding Stress, Altered Protein Homeostasis, and Feedback Regulation of Metabolism
Mol. Cell. Proteomics,
August 1, 2009;
8(8):
1789 - 1810.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Kim, A. Rudella, V. Ramirez Rodriguez, B. Zybailov, P. D. B. Olinares, and K. J. van Wijk
Subunits of the Plastid ClpPR Protease Complex Have Differential Contributions to Embryogenesis, Plastid Biogenesis, and Plant Development in Arabidopsis
PLANT CELL,
June 1, 2009;
21(6):
1669 - 1692.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Patel, S.-C. Hsu, J. Bedard, K. Inoue, and P. Jarvis
The Omp85-Related Chloroplast Outer Envelope Protein OEP80 Is Essential for Viability in Arabidopsis
Plant Physiology,
September 1, 2008;
148(1):
235 - 245.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Yu, X. Liu, M. Alsheikh, S. Park, and S. Rodermel
Mutations in SUPPRESSOR OF VARIEGATION1, a Factor Required for Normal Chloroplast Translation, Suppress var2-Mediated Leaf Variegation in Arabidopsis
PLANT CELL,
July 1, 2008;
20(7):
1786 - 1804.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
U. Flores-Perez, S. Sauret-Gueto, E. Gas, P. Jarvis, and M. Rodriguez-Concepcion
A Mutant Impaired in the Production of Plastome-Encoded Proteins Uncovers a Mechanism for the Homeostasis of Isoprenoid Biosynthetic Enzymes in Arabidopsis Plastids
PLANT CELL,
May 1, 2008;
20(5):
1303 - 1315.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Miura, Y. Kato, R. Matsushima, V. Albrecht, S. Laalami, and W. Sakamoto
The Balance between Protein Synthesis and Degradation in Chloroplasts Determines Leaf Variegation in Arabidopsis yellow variegated Mutants
PLANT CELL,
April 1, 2007;
19(4):
1313 - 1328.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. L.E. Sjogren, T. M. Stanne, B. Zheng, S. Sutinen, and A. K. Clarke
Structural and Functional Insights into the Chloroplast ATP-Dependent Clp Protease in Arabidopsis
PLANT CELL,
October 1, 2006;
18(10):
2635 - 2649.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Rudella, G. Friso, J. M. Alonso, J. R. Ecker, and K. J. van Wijk
Downregulation of ClpR2 Leads to Reduced Accumulation of the ClpPRS Protease Complex and Defects in Chloroplast Biogenesis in Arabidopsis
PLANT CELL,
July 1, 2006;
18(7):
1704 - 1721.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. I. Andersson, R. Blakytny, J. Kirstein, K. Turgay, B. Bukau, A. Mogk, and A. K. Clarke
Cyanobacterial ClpC/HSP100 Protein Displays Intrinsic Chaperone Activity
J. Biol. Chem.,
March 3, 2006;
281(9):
5468 - 5475.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Bedard and P. Jarvis
Recognition and envelope translocation of chloroplast preproteins
J. Exp. Bot.,
September 1, 2005;
56(419):
2287 - 2320.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|