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Chloroplast SRP43 acts as a chaperone for glutamyl-tRNA reductase, the rate-limiting enzyme in tetrapyrrole biosynthesis

Wang, Peng and Liang, Fu-Cheng and Wittmann, Daniel and Siegel, Alex and Shan, Shu-ou and Grimm, Bernhard (2018) Chloroplast SRP43 acts as a chaperone for glutamyl-tRNA reductase, the rate-limiting enzyme in tetrapyrrole biosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 115 (15). E3588-E3596. ISSN 0027-8424. PMCID PMC5899456. doi:10.1073/pnas.1719645115. https://resolver.caltech.edu/CaltechAUTHORS:20180326-161145347

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Abstract

Assembly of light-harvesting complexes requires synchronization of chlorophyll (Chl) biosynthesis with biogenesis of light-harvesting Chl a/b-binding proteins (LHCPs). The chloroplast signal recognition particle (cpSRP) pathway is responsible for transport of nucleus-encoded LHCPs in the stroma of the plastid and their integration into the thylakoid membranes. Correct folding and assembly of LHCPs require the incorporation of Chls, whose biosynthesis must therefore be precisely coordinated with membrane insertion of LHCPs. How the spatiotemporal coordination between the cpSRP machinery and Chl biosynthesis is achieved is poorly understood. In this work, we demonstrate a direct interaction between cpSRP43, the chaperone that mediates LHCP targeting and insertion, and glutamyl-tRNA reductase (GluTR), a rate-limiting enzyme in tetrapyrrole biosynthesis. Concurrent deficiency for cpSRP43 and the GluTR-binding protein (GBP) additively reduces GluTR levels, indicating that cpSRP43 and GBP act nonredundantly to stabilize GluTR. The substrate-binding domain of cpSRP43 binds to the N-terminal region of GluTR, which harbors aggregation-prone motifs, and the chaperone activity of cpSRP43 efficiently prevents aggregation of these regions. Our work thus reveals a function of cpSRP43 in Chl biosynthesis and suggests a striking mechanism for posttranslational coordination of LHCP insertion with Chl biosynthesis.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.1719645115DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5899456/PubMed CentralArticle
http://www.pnas.org/content/suppl/2018/03/21/1719645115.DCSupplementalPublisherSupplementary Materials
ORCID:
AuthorORCID
Wang, Peng0000-0001-8420-5326
Siegel, Alex0000-0003-3601-5178
Shan, Shu-ou0000-0002-6526-1733
Grimm, Bernhard0000-0002-9730-1074
Additional Information:© 2018 National Academy of Sciences. Published under the PNAS license. Edited by Donald R. Ort, University of Illinois at Urbana–Champaign, Urbana, IL, and approved March 7, 2018 (received for review November 13, 2017) We thank Prof. Danja Schünemann (Ruhr University Bochum) for the help with Arabidopsis cpsrp mutants, GST-cpSRP43 expression vector, and antibodies against cpSRP components. We thank Dr. B. Hedtke and J. Apitz (B.G. laboratory) for help with research materials. This work was supported by a fellowship from the Alexander von Humboldt Foundation (to P.W.) and by grants from the Betty and Gordon Moore Foundation (Grant 94-3397785) and NIH (Grant R01 GM114390) (both to S.-o.S.) and a grant from the Deutsche Forschungsgemeinschaft (FOR2092, Grant GR 936/18-1 to B.G.). Author contributions: P.W., F.-C.L., D.W., A.S., S.-o.S., and B.G. designed research; P.W., F.-C.L., D.W., and A.S. performed research; P.W., F.-C.L., D.W., A.S., S.-o.S., and B.G. analyzed data; and P.W., S.-o.S., and B.G. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1719645115/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Alexander von Humboldt FoundationUNSPECIFIED
Gordon and Betty Moore Foundation94-3397785
NIHR01 GM114390
Deutsche Forschungsgemeinschaft (DFG)GR 936/18-1
Subject Keywords:chloroplast signal recognition particle; chaperone; tetrapyrrole biosynthesis; 5-aminolevulinic acid; chloroplast biogenesis
Issue or Number:15
PubMed Central ID:PMC5899456
DOI:10.1073/pnas.1719645115
Record Number:CaltechAUTHORS:20180326-161145347
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20180326-161145347
Official Citation:Chloroplast SRP43 acts as a chaperone for glutamyl-tRNA reductase, the rate-limiting enzyme in tetrapyrrole biosynthesis Peng Wang, Fu-Cheng Liang, Daniel Wittmann, Alex Siegel, Shu-ou Shan, Bernhard Grimm Proceedings of the National Academy of Sciences Apr 2018, 115 (15) E3588-E3596; DOI: 10.1073/pnas.1719645115
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:85436
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:26 Mar 2018 23:26
Last Modified:11 Mar 2022 19:46

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