A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts

Domı́nguez-Solı́s, José R.; He, Zengyong; Lima, Amparo; Ting, Julie T. L.; Buchanan, Bob B.; Luan, Sheng

doi:10.1073/pnas.0808204105

Cited by 134 publications

(141 citation statements)

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“…S14 A and B), as previously reported (30,31,42,43). In contrast, these mutants displayed reduced growth and PSII activity in the greenhouse (SI Appendix, Fig.…”

Section: Mph2 Promotes Psii Protein Subunit Turnover and Interacts Wisupporting

confidence: 82%

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A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments

Liu

Last

2017

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

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Despite our increasingly sophisticated understanding of mechanisms ensuring efficient photosynthesis under laboratory-controlled light conditions, less is known about the regulation of photosynthesis under fluctuating light. This is important because-in naturephotosynthetic organisms experience rapid and extreme changes in sunlight, potentially causing deleterious effects on photosynthetic efficiency and productivity. Here we report that the chloroplast thylakoid lumenal protein MAINTENANCE OF PHOTOSYSTEM II UNDER HIGH LIGHT 2 (MPH2; encoded by At4g02530) is required for growth acclimation of Arabidopsis thaliana plants under controlled photoinhibitory light and fluctuating light environments. Evidence is presented that mph2 mutant light stress susceptibility results from a defect in photosystem II (PSII) repair, and our results are consistent with the hypothesis that MPH2 is involved in disassembling monomeric complexes during regeneration of dimeric functional PSII supercomplexes. Moreover, mph2-and previously characterized PSII repair-defective mutants-exhibited reduced growth under fluctuating light conditions, while PSII photoprotection-impaired mutants did not. These findings suggest that repair is not only required for PSII maintenance under static high-irradiance light conditions but is also a regulatory mechanism facilitating photosynthetic adaptation under fluctuating light environments. This work has implications for improvement of agricultural plant productivity through engineering PSII repair.fluctuating light | photosynthesis | photosystem II repair | photoprotection | chloroplast thylakoid lumen

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“…S14 A and B), as previously reported (30,31,42,43). In contrast, these mutants displayed reduced growth and PSII activity in the greenhouse (SI Appendix, Fig.…”

Section: Mph2 Promotes Psii Protein Subunit Turnover and Interacts Wisupporting

confidence: 82%

“…S1). Loss-of-function mutants in these genes all exhibit reduced PSII efficiency upon exposure to short-term or long-term high-light treatments (26)(27)(28)(29)(30)(31)(32)(33)(34).…”

Section: Identification Of a Mutant With Defects In Photosynthetic Rementioning

confidence: 99%

A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments

Liu

Last

2017

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

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“…RB60 (57) and 2-Cys Prx (58)). Another Trx target, cyclophilin 20-3 (59), which was in the reduced state when isolated, has been linked to oxidative stress (60). It is conceivable that the activity of the TIC complex is subjected both to metabolic and oxidative regulation.…”

Section: Discussionmentioning

confidence: 99%

Characterization of Tic110, a Channel-forming Protein at the Inner Envelope Membrane of Chloroplasts, Unveils a Response to Ca2+ and a Stromal Regulatory Disulfide Bridge

Balsera

Goetze

Kovács-Bogdán

et al. 2009

Journal of Biological Chemistry

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117

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Tic110 has been proposed to be a channel-forming protein at the inner envelope of chloroplasts whose function is essential for the import of proteins synthesized in the cytosol. Sequence features and topology determination experiments presently summarized suggest that Tic110 consists of six transmembrane helices. Its topology has been mapped by limited proteolysis experiments in combination with mass spectrometric determinations and cysteine modification analysis. Two hydrophobic transmembrane helices located in the N terminus serve as a signal for the localization of the protein to the membrane as shown previously. The other amphipathic transmembrane helices are located in the region composed of residues 92-959 in the pea sequence. This results in two regions in the intermembrane space localized to form supercomplexes with the TOC machinery and to receive the transit peptide of preproteins. A large region also resides in the stroma for interaction with proteins such as molecular chaperones. In addition to characterizing the topology of Tic110, we show that Ca 2؉ has a dramatic effect on channel activity in vitro and that the protein has a redox-active disulfide with the potential to interact with stromal thioredoxin.After the proposed endosymbiotic event that gave rise to chloroplasts and, as a consequence, to the massive transfer of genes from the endosymbiont to the host cell nucleus, two new machineries were developed at the outer and inner envelope of chloroplasts, the TOC and TIC complexes, respectively. The machineries transport plastid proteins, whose synthesis was moved to the cytosol, back to the plastid (for a review, see Refs. 1 and 2). Whereas the channel of the TOC complex is homologous to the Omp85 family of transporters in bacteria (3), the TIC complex shows no homology to known transport systems, since the plasma membrane-bacterial transport machineries were relocated to the thylakoid membrane. Moreover, there was an essential requirement for establishing new lines of communication between the organelle and other parts of the cell (4). In chloroplasts of land plants, redox regulation is linked to oxygen and/or light. The regulation of chloroplast-specific processes by redox in accord with the status of the organelle applies not only for transcription and translation but also for translocation. Redox regulation at the translocation level has been proposed for the TIC machinery on the basis of protein composition and dynamics (5-8) as well as specific in vitro import experiments (9). However, despite advances in our biochemical understanding of the import process, little is presently known regarding details of the role of redox or of the structure of the TIC complex, particularly with respect to its channel subunits.Tic110 is essential for protein import into plastids (10 -12). It has been proposed to be a pore-forming protein and one of the main components of the TIC complex (13). Previous studies have provided information about certain aspects of Tic110 structure-function. The region from residu...

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“…In fact, disulfide bond formation and interaction with thioredoxins has been reported to control the PPIase activity of nondivergent Cyps in animals and plants (Motohashi et al, 2003;Gourlay et al, 2007;Laxa et al, 2007). For instance, the activity of Arabidopsis CYP20-3 (ROC4), which links redox and light signals to Cys biosynthesis and stress responses in chloroplasts, is dependent on reduction by a thioredoxin (Motohashi et al, 2003;Dominguez-Solis et al, 2008).…”

Section: Cscyp Binds Selectively To a Ctd Heptad Repeatmentioning

confidence: 99%

A Redox 2-Cys Mechanism Regulates the Catalytic Activity of Divergent Cyclophilins

et al. 2013

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The citrus (Citrus sinensis) cyclophilin CsCyp is a target of the Xanthomonas citri transcription activator-like effector PthA, required to elicit cankers on citrus. CsCyp binds the citrus thioredoxin CsTdx and the carboxyl-terminal domain of RNA polymerase II and is a divergent cyclophilin that carries the additional loop KSGKPLH, invariable cysteine (Cys) residues Cys-40 and Cys-168, and the conserved glutamate (Glu) Glu-83. Despite the suggested roles in ATP and metal binding, the functions of these unique structural elements remain unknown. Here, we show that the conserved Cys residues form a disulfide bond that inactivates the enzyme, whereas Glu-83, which belongs to the catalytic loop and is also critical for enzyme activity, is anchored to the divergent loop to maintain the active site open. In addition, we demonstrate that Cys-40 and Cys-168 are required for the interaction with CsTdx and that CsCyp binds the citrus carboxyl-terminal domain of RNA polymerase II YSPSAP repeat. Our data support a model where formation of the Cys-40-Cys-168 disulfide bond induces a conformational change that disrupts the interaction of the divergent and catalytic loops, via Glu-83, causing the active site to close. This suggests a new type of allosteric regulation in divergent cyclophilins, involving disulfide bond formation and a loop-displacement mechanism.

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A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts

Cited by 134 publications

References 40 publications

A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments

A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments

Characterization of Tic110, a Channel-forming Protein at the Inner Envelope Membrane of Chloroplasts, Unveils a Response to Ca2+ and a Stromal Regulatory Disulfide Bridge

A Redox 2-Cys Mechanism Regulates the Catalytic Activity of Divergent Cyclophilins

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