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Research article

Identification of new protein substrates for the chloroplast ATP-dependent Clp protease supports its constitutive role in Arabidopsis

Tara M. Stanne, Lars L. E. Sjögren, Shai Koussevitzky, Adrian K. Clarke
Biochemical Journal Jan 01, 2009, 417 (1) 257-269; DOI: 10.1042/BJ20081146
Tara M. Stanne
Department of Plant and Environmental Sciences, Gothenburg University, Box 461, 405 30 Gothenburg, Sweden
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Lars L. E. Sjögren
Department of Plant and Environmental Sciences, Gothenburg University, Box 461, 405 30 Gothenburg, Sweden
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Shai Koussevitzky
Department of Biochemistry and Molecular Biology, University of Nevada, Mail stop 200, Reno, NV 89557-0014, U.S.A.
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Adrian K. Clarke
Department of Plant and Environmental Sciences, Gothenburg University, Box 461, 405 30 Gothenburg, Sweden
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  • For correspondence: adrian.clarke@dpes.gu.se
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Abstract

The ATP-dependent Clp protease in plant chloroplasts consists of a heterogeneous proteolytic core containing multiple ClpP and ClpR paralogues. In this study, we have examined in detail the only viable knockout mutant to date of one of these subunits in Arabidopsis thaliana, ClpR1. Loss of ClpR1 caused a slow-growth phenotype, with chlorotic leaves during early development that later partially recovered upon maturity. Analysis of the Clp proteolytic core in the clpR1 mutant (clpR1-1) revealed approx. 10% of the wild-type levels remaining, probably due to a relative increase in the closely related ClpR3 protein and its partial substitution of ClpR1 in the core complex. A proteomic approach using an in organello proteolytic assay revealed 19 new potential substrates for the chloroplast Clp protease. Many of these substrates were constitutive enzymes involved in different metabolic pathways, including photosynthetic carbon fixation, nitrogen metabolism and chlorophyll/haem biosynthesis, whereas others function in housekeeping roles such as RNA maturation, protein synthesis and maturation, and recycling processes. In contrast, degradation of the stress-related chloroplast proteins Hsp21 (heat-shock protein 21) and lipoxygenase 2 was unaffected in the clpR1-1 line and thus not facilitated by the Clp protease. Overall, we show that the chloroplast Clp protease is principally a constitutive enzyme that degrades numerous stromal proteins, a feature that almost certainly underlies its vital importance for chloroplast function and plant viability.

  • Arabidopsis thaliana
  • chloroplast
  • Clp
  • proteolysis
  • stroma

Abbreviations: BCA, bicinchoninic acid; 1D, one-dimensional; 2D, two-dimensional; DTT, dithiothreitol; EF, elongation factor; EMS, ethylmethanesulfonate; ETR, electron transport rate; FW, fresh weight; FBP ALD, fructose bisphosphate aldolase; GS2, glutamine synthetase 2; Hsp, heat-shock protein; IEF, isoelectric focusing; Lox2, lipoxygenase 2; MALDI–TOF MS, matrix-assisted laser-desorption ionization–time-of-flight MS; NDP, nucleoside diphosphate; PPIase, peptidyl-prolyl cis-trans isomerase; PS, photosystem; RH, relative humidity; Rubisco, ribulose-1,5-bisphosphate carboxylase/oxygenase; SSU, small subunit; UPRT, uracil phosphoribosyltransferase; UTase, uridylyltransferase

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January 2009

Volume: 417 Issue: 1

Biochemical Journal: 417 (1)
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Identification of new protein substrates for the chloroplast ATP-dependent Clp protease supports its constitutive role in Arabidopsis
Tara M. Stanne, Lars L. E. Sjögren, Shai Koussevitzky, Adrian K. Clarke
Biochemical Journal Jan 2009, 417 (1) 257-269; DOI: 10.1042/BJ20081146
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Identification of new protein substrates for the chloroplast ATP-dependent Clp protease supports its constitutive role in Arabidopsis
Tara M. Stanne, Lars L. E. Sjögren, Shai Koussevitzky, Adrian K. Clarke
Biochemical Journal Jan 2009, 417 (1) 257-269; DOI: 10.1042/BJ20081146

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Keywords

Arabidopsis thaliana
chloroplast
Clp
proteolysis
stroma

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