Evidence for the Existence in Arabidopsis thaliana of the Proteasome Proteolytic Pathway

Polge, Cécile; Jaquinod, Michel; Holzer, Frances M.; Bourguignon, Jacques; Walling, Linda L.; Brouquisse, Renaud

doi:10.1074/jbc.m109.035394

Cited by 103 publications

(82 citation statements)

References 65 publications

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“…The 20S proteasome subunit PAE2 was constitutively neosynthesized from 8 to 48 HAI, whereas PAB1 was neosynthesized preferentially between 8 and 24 HAI (supplemental Table S8). It has been highlighted that the degradation of carbonylated proteins is partially mediated by the 20S proteasome in accordance with the favored detection of a 20S proteasome/TPPII couple in Arabidopsis seeds (93,94).…”

Section: Discussionmentioning

confidence: 87%

“…TPPII is the main exopeptidase involved in the processing of large proteasome products and is probably necessary for efficient protein turnover (92), especially contributing to the preferential catabolism of oxidized (carbonylated) proteins (93). Given that SSPs represent the major forms of carbonylated proteins in dry mature seeds (50), it seems conceivable that TPPII might contribute to the degradation of SSPs during seed germination via the 20S proteasome pathway.…”

Section: Discussionmentioning

confidence: 99%

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Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination

Galland¹,

Huguet²,

Arc³

et al. 2014

Molecular & Cellular Proteomics

146

155

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During seed germination, the transition from a quiescent metabolic state in a dry mature seed to a proliferative metabolic state in a vigorous seedling is crucial for plant propagation as well as for optimizing crop yield. This work provides a detailed description of the dynamics of protein synthesis during the time course of germination, demonstrating that mRNA translation is both sequential and selective during this process. The complete inhibition of the germination process in the presence of the translation inhibitor cycloheximide established that mRNA translation is critical for Arabidopsis seed germination. However, the dynamics of protein turnover and the selectivity of protein synthesis (mRNA translation) during Arabidopsis seed germination have not been addressed yet. Based on our detailed knowledge of the Arabidopsis seed proteome, we have deepened our understanding of seed mRNA translation during germination by combining twodimensional gel-based proteomics with dynamic radiolabeled proteomics using a radiolabeled amino acid precursor, namely [35 S]-methionine, in order to highlight de novo protein synthesis, stability, and turnover. Our data confirm that during early imbibition, the Arabidopsis translatome keeps reflecting an embryonic maturation program until a certain developmental checkpoint. Furthermore, by dividing the seed germination time lapse into discrete time windows, we highlight precise and specific patterns of protein synthesis. These data refine and deepen our knowledge of the three classical phases of seed germination based on seed water uptake during imbibition and reveal that selective mRNA translation is a key feature of seed germination. Beyond the quantitative control of translational activity, both the selectivity of mRNA translation and protein turnover appear as specific regulatory systems, critical for timing the molecular events leading to successful germination and seedling establishment. Molecular & Cellular Proteomics 13: 10.1074/mcp.M113.032227, 252-268, 2014.Seed germination is a vital stage in the plant life cycle during which embryo cells experience a programmed transition from a quiescent to a highly active metabolic state. Accordingly, seed quality in terms of germination vigor is of paramount importance for both ecological aspects and practical applications, as it influences the level, timing, and uniformity of seedling emergence in a wide range of environmental conditions (1, 2). In efforts to decipher the complex molecular mechanisms that control seed germination, genetic, genomic, and postgenomic analyses have been developed on the model plant Arabidopsis thaliana (3-6). Germination is classically described as a sequential time course divided into three major phases of seed water uptake (7). Phase I is characterized by rapid seed imbibition, which is crucial for the transition from the quiescent metabolic state of the dry seed to the high metabolic activity of the hydrated seed. Phase II corresponds to a period during which the seed imbibition level remains const...

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Section: Discussionmentioning

confidence: 87%

Section: Discussionmentioning

confidence: 99%

Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination

Galland¹,

Huguet²,

Arc³

et al. 2014

Molecular & Cellular Proteomics

146

155

View full text Add to dashboard Cite

show abstract

“…In plants, the proteasome was identified in all species investigated so far (Smalle and Vierstra 2004). The presence of TPPII and many aminopeptidases was also reported in plants (Book et al 2005;Matsui et al 2006), and the presence of the whole proteasome pathway (also including TOP) has been recently reported in Arabidopsis leaves (Polge et al 2009). …”

Section: Introductionmentioning

confidence: 94%

Up-regulation of leucine aminopeptidase-A in cadmium-treated tomato roots

Boulila-Zoghlami

Gallusci

Holzer

et al. 2011

Planta

Self Cite

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The effects of cadmium (Cd) on aminopeptidase (AP) activities and Leucine-AP (LAP) expression were investigated in the roots of tomato (Solanum lycopersicum L., var Ibiza) plants. Three-week-old plants were grown for 10 days in the presence of 0.3-300 μM Cd and compared to control plants grown in the absence of Cd. AP activities were measured using six different p-nitroanilide (p-NA) substrates. Leu, Met, Arg, Pro and Lys hydrolyzing activities increased in roots of Cd-treated plants, while Phe-pNA cleavage was not enhanced after Cd treatments. The use of peptidase inhibitors showed that most of the Leu-pNA hydrolyzing activity was related to one or several metallo-APs. Changes in Lap transcripts, protein and activities were measured in the roots of 0 and 30-μM Cd-treated plants. LapA transcript levels increased in Cd-treated roots, whereas LapN RNAs levels were not modified. To assess amount of Leu-pNA hydrolyzing activity associated with the hexameric LAPs, LAP activity was measured following immunoprecipitation with a LAP polyclonal antiserum. LAP activity increased in Cd-treated roots. There was a corresponding increase in LAP-A protein levels detected in 2D-immunoblots. The role of LAP-A in the proteolytic response to Cd stress is discussed.

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“…In Arabidopsis, the proteasome generates short peptides 3-24 aa in length (48). It is possible that CyOP (the cytosolic paralog of OOP) is engaged in the degradation of proteasome-generated peptides as shown for cytosol-localized M3A orthologs in mammals (49).…”

Section: Discussionmentioning

confidence: 99%

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.

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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Evidence for the Existence in Arabidopsis thaliana of the Proteasome Proteolytic Pathway

Cited by 103 publications

References 65 publications

Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination

Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination

Up-regulation of leucine aminopeptidase-A in cadmium-treated tomato roots

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

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