Catalysis, Subcellular Localization, Expression and Evolution of the Targeting Peptides Degrading Protease, AtPreP2

Bhushan, Shashi; Ståhl, Anna; Nilsson, Stefan; Lefebvre, Benoît; Seki, Motoaki; Roth, Christian; McWilliam, David; Wright, Sarah; Liberles, David A.; Shinozaki, Kazuo; Bruce, Barry D.; Boutry, Marc; Glaser, Elzbieta

doi:10.1093/pcp/pci107

Cited by 57 publications

(41 citation statements)

References 55 publications

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“…The up-regulation of chaperones ClpC-1,2 was already mentioned, and in addition to a role in import, they are believed to deliver substrate to the ClpPR cores. Stromal Zn 2ϩ -proteases PreP1,2 (also named ZnMP1,2) were suggested to be involved in degradation of cleaved chloroplast transit peptides (3,68,69) and were on average 4-fold up-regulated in the seedlings, but they were unchanged in the mature chloroplast as determined by ICAT and in agreement with the colorless native PAGE analysis of mature clpr2-1 (36).…”

Section: Clpr2 Protease In a Thalianasupporting

confidence: 63%

Large Scale Comparative Proteomics of a Chloroplast Clp Protease Mutant Reveals Folding Stress, Altered Protein Homeostasis, and Feedback Regulation of Metabolism

Zybailov

Friso

Kim

et al. 2009

Molecular & Cellular Proteomics

134

149

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The clpr2-1 mutant is delayed in development due to reduction of the chloroplast ClpPR protease complex. To understand the role of Clp proteases in plastid biogenesis and homeostasis, leaf proteomes of young seedlings of clpr2-1 and wild type were compared using large scale mass spectrometry-based quantification using an LTQOrbitrap and spectral counting with significance determined by G-tests. Virtually only chloroplast-localized proteins were significantly affected, indicating that the molecular phenotype was confined to the chloroplast. A comparative chloroplast stromal proteome analysis of fully developed plants was used to complement the data set. Chloroplast unfoldase ClpB3 was strongly up-regulated in both young and mature leaves, suggesting widespread and persistent protein folding stress. The importance of ClpB3 in the clp2-1 mutant was demonstrated by the observation that a CLPR2 and CLPB3 double mutant was seedling-lethal. The observed up-regulation of chloroplast chaperones and protein sorting components further illustrated destabilization of protein homeostasis. Delayed rRNA processing and up-regulation of a chloroplast DEAD box RNA helicase and polynucleotide phosphorylase, but no significant change in accumulation of ribosomal subunits, suggested a bottleneck in ribosome assembly or RNA metabolism. Strong up-regulation of a chloroplast translational regulator TypA/BipA GTPase suggested a specific response in plastid gene expression to the distorted homeostasis. The stromal proteases PreP1,2 were up-regulated, likely constituting compensation for reduced Clp protease activity and possibly shared substrates between the ClpP and PreP protease systems. The thylakoid photosynthetic apparatus was decreased in the seedlings, whereas several structural thylakoid-associated plastoglobular proteins were strongly up-regulated. Two thylakoid-associated reductases involved in isoprenoid and chlorophyll synthesis were up-regulated reflecting feedback from rate-limiting photosynthetic electron transport. We discuss the quantitative proteomics data and the role of Clp proteolysis using a "systems view" of chloroplast homeostasis and metabolism and provide testable hypotheses and putative substrates to further determine the significance of Clp-driven proteolysis.

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Section: Clpr2 Protease In a Thalianasupporting

confidence: 63%

Large Scale Comparative Proteomics of a Chloroplast Clp Protease Mutant Reveals Folding Stress, Altered Protein Homeostasis, and Feedback Regulation of Metabolism

Zybailov

Friso

Kim

et al. 2009

Molecular & Cellular Proteomics

134

149

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“…PreP initially was identified in plant mitochondria as the protease responsible for the degradation of the presequence of the ATPase beta subunit (pF 1 β) and the chloroplastic transit peptide of the small subunit of ribulose-1,5-bisphosphate carboxylase oxygenase (18,19). Consistent with this result, A. thaliana PreP (AtPreP) was shown to have a dual localization in mitochondrial matrix and chloroplastic stroma (18,20). In addition to targeting peptides generated by processing, AtPreP1 degrades a wide range of unstructured peptides ranging from 10 from 65 aa (18).…”

mentioning

confidence: 83%

Organellar oligopeptidase (OOP) provides a complementary pathway for targeting peptide degradation in mitochondria and chloroplasts

Kmiec¹,

Teixeira²,

Berntsson³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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104

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Both mitochondria and chloroplasts contain distinct proteolytic systems for precursor protein processing catalyzed by the mitochondrial and stromal processing peptidases and for the degradation of targeting peptides catalyzed by presequence protease. Here, we have identified and characterized a component of the organellar proteolytic systems in Arabidopsis thaliana, the organellar oligopeptidase, OOP (At5g65620). OOP belongs to the M3A family of peptidedegrading metalloproteases. Using two independent in vivo methods, we show that the protease is dually localized to mitochondria and chloroplasts. Furthermore, we localized the OPP homolog At5g10540 to the cytosol. Analysis of peptide degradation by OOP revealed substrate size restriction from 8 to 23 aa residues. Short mitochondrial targeting peptides (presequence of the ribosomal protein L29 and presequence of 1-aminocyclopropane-1-carboxylic acid deaminase 1) and N-and C-terminal fragments derived from the presequence of the ATPase beta subunit ranging in size from 11 to 20 aa could be degraded. MS analysis showed that OOP does not exhibit a strict cleavage pattern but shows a weak preference for hydrophobic residues (F/L) at the P1 position. The crystal structures of OOP, at 1.8-1.9 Å, exhibit an ellipsoidal shape consisting of two major domains enclosing the catalytic cavity of 3,000 Å 3 . The structural and biochemical data suggest that the protein undergoes conformational changes to allow peptide binding and proteolysis. Our results demonstrate the complementary role of OOP in targeting-peptide degradation in mitochondria and chloroplasts.

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“…Transit peptide degradation involves one or two isoforms of the presequence peptidase (PreP1/2), which belongs to a metalloendopeptidase family (Stahl et al, 2002;Bhushan et al, 2003Bhushan et al, , 2005Moberg et al, 2003). Organellar oligopeptidase (OOP) is another zinc metalloprotease that participates in targeting peptide degradation.…”

Section: Processing Proteasesmentioning

confidence: 99%

Chloroplast Proteases: Updates on Proteolysis within and across Suborganellar Compartments

2016

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ORCID IDs: 0000-0003-1718-9121 (Y.K.); 0000-0001-9747-5042 (W.S.).Chloroplasts originated from the endosymbiosis of ancestral cyanobacteria and maintain transcription and translation machineries for around 100 proteins. Most endosymbiont genes, however, have been transferred to the host nucleus, and the majority of the chloroplast proteome is composed of nucleus-encoded proteins that are biosynthesized in the cytosol and then imported into chloroplasts. How chloroplasts and the nucleus communicate to control the plastid proteome remains an important question. Protein-degrading machineries play key roles in chloroplast proteome biogenesis, remodeling, and maintenance. Research in the past few decades has revealed more than 20 chloroplast proteases, which are localized to specific suborganellar locations. In particular, two energy-dependent processive proteases of bacterial origin, Clp and FtsH, are central to protein homeostasis. Processing endopeptidases such as stromal processing peptidase and thylakoidal processing peptidase are involved in the maturation of precursor proteins imported into chloroplasts by cleaving off the amino-terminal transit peptides. Presequence peptidases and organellar oligopeptidase subsequently degrade the cleaved targeting peptides. Recent findings have indicated that not only intraplastidic but also extraplastidic processive protein-degrading systems participate in the regulation and quality control of protein translocation across the envelopes. In this review, we summarize current knowledge of the major chloroplast proteases in terms of type, suborganellar localization, and diversification. We present details of these degradation processes as case studies according to suborganellar compartment (envelope, stroma, and thylakoids). Key questions and future directions in this field are discussed.Over 1 billion years of plastid evolution since the endosymbiosis of ancestral cyanobacteria (Douzery et al., 2004), chloroplast biogenesis has gained complexity, with large sets of the endosymbiont genes being transferred to host nuclear genomes. While only 100 endosymbiont genes remain in the plastid genome, with the corresponding proteins biosynthesized there, the nuclear genes have often gained complexity by duplication and diversification of the original endosymbiotic genes. This complexity raises numerous questions regarding (1) at what level gene expression is coordinately controlled, (2) what molecules coordinate the cross talk between chloroplasts and the nucleus, (3) how proteins get across membranes and become imported into chloroplasts, and (4) how the stoichiometries of nucleus-and chloroplast-encoded subunits within individual chloroplast protein complexes such as photosystems and Rubisco are strictly maintained.Given these questions, chloroplast biogenesis has remained a central subject in plant physiology for the last few decades (Jarvis and López-Juez, 2013). In our view, the aforementioned questions point to the importance of protein homeostasis and posttranslational modificat...

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Catalysis, Subcellular Localization, Expression and Evolution of the Targeting Peptides Degrading Protease, AtPreP2

Cited by 57 publications

References 55 publications

Large Scale Comparative Proteomics of a Chloroplast Clp Protease Mutant Reveals Folding Stress, Altered Protein Homeostasis, and Feedback Regulation of Metabolism

Large Scale Comparative Proteomics of a Chloroplast Clp Protease Mutant Reveals Folding Stress, Altered Protein Homeostasis, and Feedback Regulation of Metabolism

Organellar oligopeptidase (OOP) provides a complementary pathway for targeting peptide degradation in mitochondria and chloroplasts

Chloroplast Proteases: Updates on Proteolysis within and across Suborganellar Compartments

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