Two Paths Diverged in the Stroma: Targeting to Dual SEC Translocase Systems in Chloroplasts

Overview

Journal Photosynth Res

Publisher Springer

Date 2018 Jun 29

PMID 29951837

Citations 12

Authors

Donna E Fernandez

Affiliations

Soon will be listed here.

Abstract

Chloroplasts inherited systems and strategies for protein targeting, translocation, and integration from their cyanobacterial ancestor. Unlike cyanobacteria however, chloroplasts in green algae and plants contain two distinct SEC translocase/integrase systems: the SEC1 system in the thylakoid membrane and the SEC2 system in the inner envelope membrane. This review summarizes the mode of action of SEC translocases, identification of components of the SEC2 system, evolutionary history of SCY and SECA genes, and previous work on the co- and post-translational targeting of lumenal and thylakoid membrane proteins to the SEC1 system. Recent work identifying substrates for the SEC2 system and potential features that may contribute to inner envelope targeting are also discussed.

Citing Articles

Yellow barley xan-m mutants are deficient in the motor unit SECA1 of the SEC1 translocase system.

Stuart D, Ivanova A, Zakhrabekova S, Hansson M Planta. 2025; 261(4):68.

PMID: 40009246 PMC: 11865152. DOI: 10.1007/s00425-025-04654-9.

STIC2 selectively binds ribosome-nascent chain complexes in the cotranslational sorting of Arabidopsis thylakoid proteins.

Stolle D, Osterhoff L, Treimer P, Lambertz J, Karstens M, Keller J EMBO J. 2024; 43(20):4699-4719.

PMID: 39192033 PMC: 11480477. DOI: 10.1038/s44318-024-00211-4.

Plastid Molecular Chaperone HSP90C Interacts with the SecA1 Subunit of Sec Translocase for Thylakoid Protein Transport.

Nair A, Jiang T, Mu B, Zhao R Plants (Basel). 2024; 13(9).

PMID: 38732479 PMC: 11085213. DOI: 10.3390/plants13091265.

Thylakoid protein FPB1 synergistically cooperates with PAM68 to promote CP47 biogenesis and Photosystem II assembly.

Zhang L, Ruan J, Gao F, Xin Q, Che L, Cai L Nat Commun. 2024; 15(1):3122.

PMID: 38600073 PMC: 11006888. DOI: 10.1038/s41467-024-46863-y.

Chloroplast protein translocation pathways and ubiquitin-dependent regulation at a glance.

Nellaepalli S, Lau A, Jarvis R J Cell Sci. 2023; 136(18).

PMID: 37732520 PMC: 10546890. DOI: 10.1242/jcs.241125.

References

Voelker R, Barkan A . Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid. EMBO J. 1995; 14(16):3905-14. PMC: 394469. DOI: 10.1002/j.1460-2075.1995.tb00062.x. View

Schuenemann D, Amin P, Hartmann E, Hoffman N . Chloroplast SecY is complexed to SecE and involved in the translocation of the 33-kDa but not the 23-kDa subunit of the oxygen-evolving complex. J Biol Chem. 1999; 274(17):12177-82. DOI: 10.1074/jbc.274.17.12177. View

Tripp J, Inoue K, Keegstra K, Froehlich J . A novel serine/proline-rich domain in combination with a transmembrane domain is required for the insertion of AtTic40 into the inner envelope membrane of chloroplasts. Plant J. 2007; 52(5):824-38. DOI: 10.1111/j.1365-313X.2007.03279.x. View

Haward S, Napier J, Gray J . Chloroplast SecA functions as a membrane-associated component of the Sec-like protein translocase of pea chloroplasts. Eur J Biochem. 1997; 248(3):724-30. DOI: 10.1111/j.1432-1033.1997.00724.x. View

Williams-Carrier R, Stiffler N, Belcher S, Kroeger T, Stern D, Monde R . Use of Illumina sequencing to identify transposon insertions underlying mutant phenotypes in high-copy Mutator lines of maize. Plant J. 2010; 63(1):167-77. DOI: 10.1111/j.1365-313X.2010.04231.x. View

Bohnert M, Rehling P, Guiard B, Herrmann J, Pfanner N, van der Laan M . Cooperation of stop-transfer and conservative sorting mechanisms in mitochondrial protein transport. Curr Biol. 2010; 20(13):1227-32. DOI: 10.1016/j.cub.2010.05.058. View

Collinson I, Corey R, Allen W . Channel crossing: how are proteins shipped across the bacterial plasma membrane?. Philos Trans R Soc Lond B Biol Sci. 2015; 370(1679). PMC: 4632601. DOI: 10.1098/rstb.2015.0025. View

Rohl T, van Wijk K . In vitro reconstitution of insertion and processing of cytochrome f in a homologous chloroplast translation system. J Biol Chem. 2001; 276(38):35465-72. DOI: 10.1074/jbc.M103005200. View

Park E, Menetret J, Gumbart J, Ludtke S, Li W, Whynot A . Structure of the SecY channel during initiation of protein translocation. Nature. 2013; 506(7486):102-6. PMC: 3948209. DOI: 10.1038/nature12720. View

10.

Jansen R, Cai Z, Raubeson L, Daniell H, dePamphilis C, Leebens-Mack J . Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci U S A. 2007; 104(49):19369-74. PMC: 2148296. DOI: 10.1073/pnas.0709121104. View

11.

Andersson H, von Heijne G . Sec dependent and sec independent assembly of E. coli inner membrane proteins: the topological rules depend on chain length. EMBO J. 1993; 12(2):683-91. PMC: 413254. DOI: 10.1002/j.1460-2075.1993.tb05702.x. View

12.

Aldridge C, Cain P, Robinson C . Protein transport in organelles: Protein transport into and across the thylakoid membrane. FEBS J. 2009; 276(5):1177-86. DOI: 10.1111/j.1742-4658.2009.06875.x. View

13.

Heijne G . The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J. 1986; 5(11):3021-7. PMC: 1167256. DOI: 10.1002/j.1460-2075.1986.tb04601.x. View

14.

Lubeck J, Heins L, Soll J . A nuclear-coded chloroplastic inner envelope membrane protein uses a soluble sorting intermediate upon import into the organelle. J Cell Biol. 1997; 137(6):1279-86. PMC: 2132540. DOI: 10.1083/jcb.137.6.1279. View

15.

Zimmer J, Nam Y, Rapoport T . Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature. 2008; 455(7215):936-43. PMC: 7164768. DOI: 10.1038/nature07335. View

16.

Yuan J, Cline K . Plastocyanin and the 33-kDa subunit of the oxygen-evolving complex are transported into thylakoids with similar requirements as predicted from pathway specificity. J Biol Chem. 1994; 269(28):18463-7. View

17.

Skalitzky C, Martin J, Harwood J, Beirne J, Adamczyk B, Heck G . Plastids contain a second sec translocase system with essential functions. Plant Physiol. 2010; 155(1):354-69. PMC: 3075773. DOI: 10.1104/pp.110.166546. View

18.

ROY L, Barkan A . A SecY homologue is required for the elaboration of the chloroplast thylakoid membrane and for normal chloroplast gene expression. J Cell Biol. 1998; 141(2):385-95. PMC: 2148445. DOI: 10.1083/jcb.141.2.385. View

19.

Karnauchov I, Cai D, Schmidt I, Herrmann R, Klosgen R . The thylakoid translocation of subunit 3 of photosystem I, the psaF gene product, depends on a bipartite transit peptide and proceeds along an azide-sensitive pathway. J Biol Chem. 1994; 269(52):32871-8. View

20.

Li Y, Singhal R, Taylor I, McMinn P, Chua X, Cline K . The Sec2 translocase of the chloroplast inner envelope contains a unique and dedicated SECE2 component. Plant J. 2015; 84(4):647-58. DOI: 10.1111/tpj.13028. View