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PMID: 10634907 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants.

The Plant cell ·Vol. 12 ·No. 1 ·2000-01-00 ·Pages 53-64

May T, Soll J

Abstract

Transit sequences of chloroplast-destined precursor proteins are phosphorylated on a serine or threonine residue. The amino acid motif around the phosphorylation site is related to the phosphopeptide binding motif for 14-3-3 proteins. Plant 14-3-3 proteins interact specifically with wheat germ lysate-synthesized chloroplast precursor proteins and require an intact phosphorylation motif within the transit sequence. Chloroplast precursor proteins do not interact with 14-3-3 when synthesized in the heterologous reticulocyte lysate. In contrast, a precursor protein destined for plant mitochondria was found to be associated with 14-3-3 proteins present in the reticulocyte lysate but not with 14-3-3 from wheat germ lysate. This indicates an unrecognized selectivity of 14-3-3 proteins for precursors from mitochondria and plastids in plants in comparison to fungi and animals. The heterooligomeric complex has an apparent size of 200 kD. In addition to the precursor protein, it contains 14-3-3 (probably as a dimer) and a heat shock protein Hsp70 isoform. Dissociation of the precursor complex requires ATP. Protein import experiments of precursor from the oligomeric complex into intact pea chloroplasts reveal three- to fourfold higher translocation rates compared with the free precursor, which is not complexed. We conclude that the 14-3-3-Hsp70-precursor protein complex is a bona fide intermediate in the in vivo protein import pathway in plants.

MeSH Terms
14-3-3 Proteins Amino Acid Motifs Amino Acid Sequence Animals Binding Sites Chloroplasts/metabolism HSP70 Heat-Shock Proteins/chemistry,genetics,metabolism In Vitro Techniques Macromolecular Substances Molecular Weight Phosphorylation Plant Proteins/chemistry,genetics,metabolism Protein Precursors/chemistry,genetics,metabolism Proteins/chemistry,genetics,metabolism Reticulocytes/metabolism Sequence Homology, Amino Acid Triticum/genetics,metabolism Tyrosine 3-Monooxygenase
Chemicals
14-3-3 Proteins HSP70 Heat-Shock Proteins Macromolecular Substances Plant Proteins Protein Precursors Proteins Tyrosine 3-Monooxygenase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
May T
Botanisches Institut der Christian-Albrechts-Universität zu Kiel, Am Botanischen Garten 1-9, D-24118 Kiel, Germany.
Soll J
References (44)
44 references, click to expand
  1. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine.
    Cell. 1996 Mar 22;84(6):889-97 PMID: 8601312
  2. Maintenance of G2 arrest in the Xenopus oocyte: a role for 14-3-3-mediated inhibition of Cdc25 nuclear import.
    EMBO J. 1999 Apr 15;18(8):2174-83 PMID: 10205171
  3. The Arabidopsis 14-3-3 multigene family.
    Plant Physiol. 1997 Aug;114(4):1421-31 PMID: 9276953
  4. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  5. 14-3-3 PROTEINS AND SIGNAL TRANSDUCTION.
    Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:49-73 PMID: 15012282
  6. A protein import receptor in pea chloroplasts, Toc86, is only a proteolytic fragment of a larger polypeptide.
    FEBS Lett. 1998 Dec 11;441(1):59-62 PMID: 9877165
  7. 14-3-3 proteins: eukaryotic regulatory proteins with many functions.
    Plant Mol Biol. 1999 Jul;40(4):545-54 PMID: 10480379
  8. Binding of purified 14-3-3 zeta signaling protein to discrete amino acid sequences within the cytoplasmic domain of the platelet membrane glycoprotein Ib-IX-V complex.
    Biochemistry. 1998 Jan 13;37(2):638-47 PMID: 9425086
  9. Molecular chaperones.
    Annu Rev Biochem. 1991;60:321-47 PMID: 1679318
  10. Characterization and isolation of the chloroplast protein import machinery.
    Methods Cell Biol. 1995;50:255-67 PMID: 8531798
  11. Protein import into chloroplasts.
    Trends Cell Biol. 1999 Jun;9(6):222-7 PMID: 10354568
  12. 14-3-3 and its possible role in co-ordinating multiple signalling pathways.
    Trends Cell Biol. 1996 Sep;6(9):341-7 PMID: 15157431
  13. p34cdc2-mediated phosphorylation at T124 inhibits nuclear import of SV-40 T antigen proteins.
    J Cell Biol. 1991 Dec;115(5):1203-12 PMID: 1659575
  14. Reconstitution of the initial steps of mitochondrial protein import.
    Nature. 1995 Aug 24;376(6542):705-9 PMID: 7651521
  15. The role of phosphorylation and the CDC28 protein kinase in cell cycle-regulated nuclear import of the S. cerevisiae transcription factor SWI5.
    Cell. 1991 Aug 23;66(4):743-58 PMID: 1652372
  16. Presequence binding factor-dependent and -independent import of proteins into mitochondria.
    J Biol Chem. 1992 Jul 5;267(19):13119-22 PMID: 1618812
  17. The rate of nuclear cytoplasmic protein transport is determined by the casein kinase II site flanking the nuclear localization sequence of the SV40 T-antigen.
    EMBO J. 1991 Mar;10(3):633-9 PMID: 1848177
  18. Phosphorylation on protein kinase C sites inhibits nuclear import of lamin B2.
    J Cell Biol. 1993 Mar;120(6):1293-304 PMID: 8449977
  19. Two components of the chloroplast protein import apparatus, IAP86 and IAP75, interact with the transit sequence during the recognition and translocation of precursor proteins at the outer envelope.
    J Cell Biol. 1996 Jul;134(2):315-27 PMID: 8707818
  20. A mitochondrial import factor purified from rat liver cytosol is an ATP-dependent conformational modulator for precursor proteins.
    EMBO J. 1993 Apr;12(4):1579-86 PMID: 8096814
  21. A constituent of the chloroplast import complex represents a new type of GTP-binding protein.
    Plant J. 1995 Mar;7(3):401-11 PMID: 7757113
  22. Functional domains of the ferredoxin transit sequence involved in chloroplast import.
    J Biol Chem. 1995 Feb 24;270(8):3882-93 PMID: 7876133
  23. Photoaffinity Labeling of Mature and Precursor Forms of the Small Subunit of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase after Expression in Escherichia coli.
    Plant Physiol. 1992 Feb;98(2):546-53 PMID: 16668675
  24. The structural basis for 14-3-3:phosphopeptide binding specificity.
    Cell. 1997 Dec 26;91(7):961-71 PMID: 9428519
  25. Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly.
    Science. 1990 May 18;248(4957):850-4 PMID: 2188360
  26. Protein import and routing systems of chloroplasts.
    Plant Cell. 1999 Apr;11(4):557-70 PMID: 10213778
  27. A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides.
    Nature. 1988 Apr 28;332(6167):800-5 PMID: 3282178
  28. Mft52, an acid-bristle protein in the cytosol that delivers precursor proteins to yeast mitochondria.
    J Biol Chem. 1997 Feb 21;272(8):5320-5 PMID: 9030606
  29. A plant homologue to mammalian brain 14-3-3 protein and protein kinase C inhibitor.
    FEBS Lett. 1992 Jan 20;296(2):222-4 PMID: 1733782
  30. Preparation of a cell-free protein-synthesizing system from wheat germ.
    Methods Enzymol. 1983;101:635-44 PMID: 6888279
  31. Analysis of the interactions of preproteins with the import machinery over the course of protein import into chloroplasts.
    J Cell Biol. 1997 Dec 29;139(7):1677-85 PMID: 9412463
  32. Different in vitro and in vivo targeting properties of the transit peptide of a chloroplast envelope inner membrane protein.
    J Biol Chem. 1997 Jun 13;272(24):15264-9 PMID: 9182551
  33. Binding of mitochondrial precursor proteins to the cytoplasmic domains of the import receptors Tom70 and Tom20 is determined by cytoplasmic chaperones.
    EMBO J. 1997 Jul 16;16(14):4267-75 PMID: 9250670
  34. Phosphorylation of the transit sequence of chloroplast precursor proteins.
    J Biol Chem. 1996 Mar 15;271(11):6545-54 PMID: 8626459
  35. Reconstitution of a chloroplast protein import channel.
    EMBO J. 1997 Dec 15;16(24):7351-60 PMID: 9405364
  36. A nuclear gene encoding the beta subunit of the mitochondrial ATP synthase in Nicotiana plumbaginifolia.
    EMBO J. 1985 Sep;4(9):2159-65 PMID: 2866954
  37. The yeast nascent polypeptide-associated complex initiates protein targeting to mitochondria in vivo.
    Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2296-301 PMID: 9482879
  38. Multiple pathways for protein transport into or across the thylakoid membrane.
    EMBO J. 1993 Nov;12(11):4105-14 PMID: 8223427
  39. Crystal structure of the zeta isoform of the 14-3-3 protein.
    Nature. 1995 Jul 13;376(6536):191-4 PMID: 7603574
  40. Envelope membrane proteins that interact with chloroplastic precursor proteins.
    Plant Cell. 1994 Jan;6(1):93-105 PMID: 8130644
  41. Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways.
    Nature. 1995 Jul 13;376(6536):188-91 PMID: 7603573
  42. Seventy-kilodalton heat shock proteins and an additional component from reticulocyte lysate stimulate import of M13 procoat protein into microsomes.
    EMBO J. 1988 Sep;7(9):2875-80 PMID: 3181144
  43. Import of proteins into mitochondria and chloroplasts.
    Trends Cell Biol. 1997 Mar;7(3):103-6 PMID: 17708917
  44. 14-3-3 proteins: a highly conserved, widespread family of eukaryotic proteins.
    Trends Biochem Sci. 1992 Dec;17(12):498-501 PMID: 1471260
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.12.1.53
Published
2000-01-00
Pages
53-64
Language
English
Region
England
NLM ID
9208688
PMCID
PMC140214
Subset
IM
External Links
PubMed source DOI: 10.1105/tpc.12.1.53 PMC Full Text View journal details
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