The POTRA domains of Toc75 exhibit chaperone-like function to facilitate import into chloroplasts

O'Neil, Patrick K.; Richardson, Lynn G.L.; Paila, Yamuna Devi; Piszczek, Grzegorz; Chakravarthy, Srinivas; Noinaj, Nicholas; Schnell, Danny J.

doi:10.1073/pnas.1621179114

Cited by 42 publications

(33 citation statements)

References 79 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The changes in dimerization could be sufficient to promote transit peptide insertion even in the absence of nucleotide exchange. It has also been shown that the intermembrane space-localized POTRA domains of Toc75 possess a transit peptide binding site (Paila et al, 2016;O'Neil et al, 2017), which could serve as a docking site for the transit peptide in the intermembrane space and reduce backsliding out of the channel in the absence of energy. In mitochondrial protein import, it has been shown that Figure 6.…”

Section: Discussionmentioning

confidence: 99%

“…The receptors are associated with Toc75, a β-barrel outer membrane protein, which forms the channel through which preproteins are translocated across the outer membrane (Schnell et al, 1994;Hinnah et al, 2002;Day et al, 2014). Toc75 is also proposed to interact with preproteins in the intermembrane space via its POTRA (polypeptide-transport associated) domains (Chen et al, 2016;Paila et al, 2016;O'Neil et al, 2017), as the POTRAs bind to preproteins and possess molecular chaperone activity in vitro (O'Neil et al, 2017). In addition, the POTRAs interact with two putative chaperones in the intermembrane space, Tic22-III and Tic22-IV, leading to the hypothesis that the Toc75 POTRAs and Tic22 proteins function coordinately to facilitate transit of the preprotein across the intermembrane space (Paila et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Molecular Topology of the Transit Peptide during Chloroplast Protein Import

et al. 2018

View full text Add to dashboard Cite

Chloroplast protein import is directed by the interaction of the targeting signal (transit peptide) of nucleus-encoded preproteins with translocons at the outer (TOC) and inner (TIC) chloroplast envelope membranes. Studies of the energetics and determinants of transit peptide binding have led to the hypothesis that import occurs through sequential recognition of transit peptides by components of TOC and TIC during protein import. To test this hypothesis, we employed a site-specific cross-linking approach to map transit peptide topology in relation to TOC-TIC components at specific stages of import in and pea (). We demonstrate that the transit peptide is in contact with Tic20 at the inner envelope in addition to TOC complex components at the earliest stages of chloroplast binding. Low levels of ATP hydrolysis catalyze the commitment of the preprotein to import by promoting further penetration across the envelope membranes and stabilizing the association of the preprotein with TOC-TIC. GTP hydrolysis at the TOC receptors serves as a checkpoint to regulate the ATP-dependent commitment of the preprotein to import and is not essential to drive preprotein import. Our results demonstrate the close cooperativity of the TOC and TIC machinery at each stage of transit peptide recognition and membrane translocation during protein import.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Molecular Topology of the Transit Peptide during Chloroplast Protein Import

et al. 2018

View full text Add to dashboard Cite

show abstract

“…cpHsp70, Hsp90C) or a 2 MDa Ycf2-FtsHi complex. The Tic40 and Tic110 proteins are also involved in the import process, and may operate downstream in soluble N-terminal polypeptide transport-associated (POTRA) domain [52], which in the case of Toc75 extends into the intermembrane space (IMS) and performs a proposed chaperone-like role [53]. The Toc75 channel has been found to reach a maximum diameter of 30 Å [54].…”

Section: Part 1 Ofmentioning

confidence: 99%

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

Thomson

Pulido

Jarvis

2020

Biochemical Society Transactions

View full text Add to dashboard Cite

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.

show abstract

“…The POTRA repeat containing domain of eukaryotic and prokaryotic Omp85 proteins was proven to bind to non‐native porins and to peptides mimicking nascent unfolded OMPs (Voulhoux et al , ; Bredemeier et al , ; Kim et al , ; Knowles et al , ). Recently, a chaperone or holdase‐like function has been proposed for the POTRA domains (O'Neil et al , ). Experimentally determined and modeled structures of BamA and BAM revealed the existence of an open and a closed BamA conformation.…”

Section: Introductionmentioning

confidence: 99%

Tic22 from Anabaena sp. PCC 7120 with holdase function involved in outer membrane protein biogenesis shuttles between plasma membrane and Omp85

Brouwer

Ngo

Yadav

et al. 2019

Molecular Microbiology

View full text Add to dashboard Cite

β-barrel-shaped outer membrane proteins (OMPs) ensure regulated exchange of molecules across the cell-wall of Gram-negative bacteria. They are synthesized in the cytoplasm and translocated across the plasma membrane via the SEC translocon. In the periplasm, several proteins participate in the transfer of OMPs to the outer membrane-localized complex catalyzing their insertion. This process has been described in detail for proteobacteria and some molecular components are conserved in cyanobacteria. For example, Omp85 proteins that catalyze the insertion of OMPs into the outer membrane exist in cyanobacteria as well. In turn, SurA and Skp involved in OMP transfer from plasma membrane to Omp85 in E. coli are likely replaced by Tic22 in cyanobacteria. We describe that anaTic22 functions as periplasmic holdase for OMPs in Anabaena sp. PCC 7120 and provide evidence for the process of substrate delivery to ana Omp85. Ana Tic22 binds to the plasma membrane with specificity for phosphatidylglycerol and monogalactosyldiacylglycerol. Substrate recognition induces membrane dissociation and interaction with the N-terminal POTRA domain of Omp85. This leads to substrate release by the interaction with a proline-rich domain and the first POTRA domain of Omp85. The order of events during OMP transfer from plasma membrane to Omp85 in cyanobacteria is discussed. Abbreviations: BAM, β-barrel assembly machinery; DGDG, digalactosyldiacylglycerol; MGDG, monogalactosyldiacylglycerol; OM, outer membrane; OMP, OM proteins; PC, phosphatidylcholine; PG, phosphatidylglycerol; PGL, peptidoglycan layer; PM, plasma membrane; POTRA, polypeptide-transportassociated domains; SQDG, sulfoquinovosyldiacylglycerol; TIC, translocon of the inner envelope membrane of chloroplasts.

show abstract

The POTRA domains of Toc75 exhibit chaperone-like function to facilitate import into chloroplasts

Cited by 42 publications

References 79 publications

Molecular Topology of the Transit Peptide during Chloroplast Protein Import

Molecular Topology of the Transit Peptide during Chloroplast Protein Import

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

Tic22 from Anabaena sp. PCC 7120 with holdase function involved in outer membrane protein biogenesis shuttles between plasma membrane and Omp85

Contact Info

Product

Resources

About