First published online June 9, 2006; 10.1105/tpc.106.042861
The Plant Cell 18:1704-1721 (2006)
© 2006 American Society of Plant Biologists
Downregulation of ClpR2 Leads to Reduced Accumulation of the ClpPRS Protease Complex and Defects in Chloroplast Biogenesis in Arabidopsis[W]
Andrea Rudellaa,
Giulia Frisoa,
Jose M. Alonsob,
Joseph R. Eckerc and
Klaas J. van Wijka,1
a Department of Plant Biology, Cornell University, Ithaca, New York 14853
b Department of Genetics, North Carolina State University, Raleigh, North Carolina 27695
c Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, California 92037
1 To whom correspondence should be addressed. E-mail kv35{at}cornell.edu; fax 607-255-3664.
Plastids contain tetradecameric Clp protease core complexes, with five ClpP Ser-type proteases, four nonproteolytic ClpR, and two associated ClpS proteins. Accumulation of total ClpPRS complex decreased twofold to threefold in an Arabidopsis thaliana T-DNA insertion mutant in CLPR2 designated clpr2-1. Differential stable isotope labeling of the ClpPRS complex with iTRAQ revealed a fivefold reduction in assembled ClpR2 accumulation and twofold to fivefold reductions in the other subunits. A ClpR2:(his)6 fusion protein that incorporated into the chloroplast ClpPRS complex fully complemented clpr2-1. The reduced accumulation of the ClpPRS protease complex led to a pale-green phenotype with delayed shoot development, smaller chloroplasts, decreased thylakoid accumulation, and increased plastoglobule accumulation. Stromal ClpC1 and 2 were both recruited to the thylakoid surface in clpr2-1. The thylakoid membrane of clpr2-1 showed increased carotenoid content, partial inactivation of photosystem II, and upregulated thylakoid proteases and stromal chaperones, suggesting an imbalance in chloroplast protein homeostasis and a well-coordinated network of proteolysis and chaperone activities. Interestingly, a subpopulation of PsaF and several light-harvesting complex II proteins accumulated in the thylakoid with unprocessed chloroplast transit peptides. We conclude that ClpR2 cannot be functionally replaced by other ClpP/R homologues and that the ClpPRS complex is central to chloroplast biogenesis, thylakoid protein homeostasis, and plant development.
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