Unraveling Hidden Components of the Chloroplast Envelope Proteome: Opportunities and Limits of Better MS Sensitivity

Bouchnak, Imen; Brugière, Sabine; Moyet, Lucas; Gall, Sophie Le; Salvi, Daniel; Kuntz, Marcel; Tardif, Marianne; Rolland, Norbert

doi:10.1074/mcp.ra118.000988

Cited by 57 publications

(63 citation statements)

References 90 publications

(164 reference statements)

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“…Thus, FBN3a (At3g26070), FBN3b (At3g26080), FBN6 (At5g19940), FBNlike (At1g18060), and probably FBN9 (At4g00030) were found to be thylakoid-localized, FBN5 (At5g09820) and a truncated version of FBN7a (At3g58010) are located in the chloroplast stroma, and FBN10 (At1g51110) in thylakoids and plastoglobules. Furthermore, FBN6 is the only isoform that was found to be enriched in purified envelope fractions (Ferro et al, 2010;Bouchnak et al, 2019). Furthermore, FBN6 is the only isoform that was found to be enriched in purified envelope fractions (Ferro et al, 2010;Bouchnak et al, 2019).…”

Section: Introductionmentioning

confidence: 94%

“…FBN6 is localized to thylakoid and envelope membranes FBN6, together with FBN3a, FBN3b, FBN-like, and most probably FBN9, was found to be thylakoid localized (Lundquist et al, 2012). Moreover, FBN6 is the only FBN isoform that was found to be enriched in purified envelope fractions (Ferro et al, 2010), a localization that was recently supported by Bouchnak et al (2019). To experimentally test for the subcellular location of FBN6, the fluorescence distribution in Col-0 protoplasts overexpressing the FBN6-eGFP fusion was investigated.…”

Section: Photosynthetic Properties Of Fbn6-1 Mutant Plantsmentioning

confidence: 99%

“…The remaining seven FBNs are localized to the plastoglobule core proteome, which in total comprises 30 proteins (Lundquist et al, 2012). Furthermore, FBN6 is the only isoform that was found to be enriched in purified envelope fractions (Ferro et al, 2010;Bouchnak et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Lack of FIBRILLIN6 in Arabidopsis thaliana affects light acclimation and sulfate metabolism

et al. 2019

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Arabidopsis thaliana contains 13 fibrillins (FBNs), which are all localized to chloroplasts. FBN1 and FBN2 are involved in photoprotection of photosystem II, and FBN4 and FBN5 are thought to be involved in plastoquinone transport and biosynthesis, respectively. The functions of the other FBNs remain largely unknown.To gain insight into the function of FBN6, we performed coexpression and Western analyses, conducted fluorescence and transmission electron microscopy, stained reactive oxygen species (ROS), measured photosynthetic parameters and glutathione levels, and applied transcriptomics and metabolomics.Using coexpression analyses, FBN6 was identified as a photosynthesis-associated gene. FBN6 is localized to thylakoid and envelope membranes, and its knockout results in stunted plants. The delayed-growth phenotype cannot be attributed to altered basic photosynthesis parameters or a reduced CO 2 assimilation rate. Under moderate light stress, primary leaves of fbn6 plants begin to bleach and contain enlarged plastoglobules. RNA sequencing and metabolomics analyses point to an alteration in sulfate reduction in fbn6. Indeed, glutathione content is higher in fbn6, which in turn confers cadmium tolerance of fbn6 seedlings.We conclude that loss of FBN6 leads to perturbation of ROS homeostasis. FBN6 enables plants to cope with moderate light stress and affects cadmium tolerance.

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Section: Introductionmentioning

confidence: 94%

Section: Photosynthetic Properties Of Fbn6-1 Mutant Plantsmentioning

confidence: 99%

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Lack of FIBRILLIN6 in Arabidopsis thaliana affects light acclimation and sulfate metabolism

et al. 2019

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“…CDC48 functions in a variety of cellular activities beyond protein homeostasis, such as cell cycle regulation and autophagy, but it is especially well known as the core motor component in ERAD [118]. Of the five reported homologues of CDC48 in Arabidopsis, CDC48A was found to associate with Toc33 [114], and has recently been identified by proteomic analysis of the chloroplast envelope [119]. Reconstitution experiments demonstrated that CDC48 operates as a cytosolic motor to retrotranslocate ubiquitinated TOC proteins prior to their degradation, a process in which SP2 was also shown to be critical [114] (Figure 1).…”

Section: Chloroplast-associated Protein Degradationmentioning

confidence: 99%

Protein import into chloroplasts and its regulation by the ubiquitin-proteasome system

Thomson

Pulido

Jarvis

2020

Biochemical Society Transactions

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Chloroplasts are photosynthetic plant organelles descended from a bacterial ancestor. The vast majority of chloroplast proteins are synthesized in the cytosol and then imported into the chloroplast post-translationally. Translocation complexes exist in the organelle's outer and inner envelope membranes (termed TOC and TIC, respectively) to facilitate protein import. These systems recognize chloroplast precursor proteins and mediate their import in an energy-dependent manner. However, many unanswered questions remain regarding mechanistic details of the import process and the participation and functions of individual components; for example, the cytosolic events that mediate protein delivery to chloroplasts, the composition of the TIC apparatus, and the nature of the protein import motor all require resolution. The flux of proteins through TOC and TIC varies greatly throughout development and in response to specific environmental cues. The import process is, therefore, tightly regulated, and it has emerged that the ubiquitin-proteasome system (UPS) plays a key role in this regard, acting at several different steps in the process. The UPS is involved in: the selective degradation of transcription factors that co-ordinate the expression of chloroplast precursor proteins; the removal of unimported chloroplast precursor proteins in the cytosol; the inhibition of chloroplast biogenesis pre-germination; and the reconfiguration of the TOC apparatus in response to developmental and environmental signals in a process termed chloroplast-associated protein degradation. In this review, we highlight recent advances in our understanding of protein import into chloroplasts and how this process is regulated by the UPS.

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“…(ii) More than 100 nucleus-encoded transporters or transporter components were detected in comparable amounts of PM samples showing that our method is feasible to detect this group of proteins. (iii) IM transporters were repeatedly identified in comparable analyses of cyanobacterial(43)(44)(45)(46)(47) or plastidial membrane fractions(48)(49)(50). Thus, a mechanism to insert nucleus-encoded multi-spanning TM proteins into chromatophore IM and thylakoids likely has not evolved (yet) in P. chromatophora.…”

mentioning

confidence: 99%

The puzzle of metabolite exchange and identification of putative octotrico peptide repeat expression regulators in the nascent photosynthetic organelles ofPaulinella chromatophora

Oberleitner

Poschmann

Macorano

et al. 2020

Preprint

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The cercozoan amoeba Paulinella chromatophora contains photosynthetic organelles - termed chromatophores - that evolved from a cyanobacterium, independently from plastids in plants and algae. Despite the more recent origin of the chromatophore, it shows tight integration into the host cell. It imports hundreds of nucleus-encoded proteins, and diverse metabolites are exchanged across the two chromatophore envelope membranes. However, the limited set of chromatophore-encoded transporters appears insufficient for supporting metabolic connectivity or protein import. Furthermore, chromatophore-localized biosynthetic pathways as well as multiprotein complexes include proteins of dual genetic origin, suggesting coordination of gene expression levels between chromatophore and nucleus. These findings imply that similar to the situation in mitochondria and plastids, nuclear factors evolved that control metabolite exchange and gene expression in the chromatophore. Here we show by mass spectrometric analyses of enriched insoluble protein fractions that, unexpectedly, nucleus-encoded transporters are not inserted into the chromatophore inner envelope membrane. Thus, despite the apparent maintenance of its barrier function, canonical metabolite transporters are missing in this membrane. Instead we identified several expanded groups of short chromatophore-targeted orphan proteins. Members of one of these groups are characterized by a single transmembrane helix, and others contain amphipathic helices. We hypothesize that these proteins are involved in modulating membrane permeability. Furthermore, we identified an expanded family of chromatophore-targeted helical repeat proteins. These proteins show similar domain architectures as known organelle-targeted octotrico peptide repeat expression regulators in algae and plants suggesting their convergent evolution as nuclear regulators of gene expression levels in the chromatophore.ImportanceThe endosymbiotic acquisition of mitochondria and plastids >1 billion years ago was central for the evolution of eukaryotic life. However, owing to their ancient origin, these organelles provide only limited insights into the initial stages of organellogenesis. The chromatophore in Paulinella evolved ~100 million years ago and thus, offers the possibility to gain valuable insights into early stages and common rules in organelle evolution. Critical to organellogenesis appears to be the establishment of nuclear control over metabolite exchange and gene expression in the endosymbiont. Here we show that the mechanism generating metabolic connectivity of the chromatophore fundamentally differs from the one for mitochondria and plastids, but likely rather resembles the poorly understood mechanism in various bacterial endosymbionts in plants and insects. Furthermore, we describe a novel class of chromatophore-targeted helical repeat proteins which evolved convergently to plastid-targeted expression regulators and are likely involved in gene expression control in the chromatophore.

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Unraveling Hidden Components of the Chloroplast Envelope Proteome: Opportunities and Limits of Better MS Sensitivity

Cited by 57 publications

References 90 publications

Lack of FIBRILLIN6 in Arabidopsis thaliana affects light acclimation and sulfate metabolism

Lack of FIBRILLIN6 in Arabidopsis thaliana affects light acclimation and sulfate metabolism

Protein import into chloroplasts and its regulation by the ubiquitin-proteasome system

The puzzle of metabolite exchange and identification of putative octotrico peptide repeat expression regulators in the nascent photosynthetic organelles ofPaulinella chromatophora

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