Abstract
The interactions of precursor proteins with components of the chloroplast envelope were investigated during the early stages of protein import using a chemical cross-linking strategy. In the absence of energy, two components of the outer envelope import machinery, IAP86 and IAP75, cross-linked to the transit sequence of the precursor to the small subunit of ribulose-1, 5-bisphosphate carboxylase (pS) in a precursor binding assay. In the presence of concentrations of ATP or GTP that support maximal precursor binding to the envelope, cross-linking to the transit sequence occurred predominantly with IAP75 and a previously unidentified 21-kD polypeptide of the inner membrane, indicating that the transit sequence had inserted across the outer membrane. Cross-linking of envelope components to sequences in the mature portion of a second precursor, preferredoxin, was detected in the presence of ATP or GTP, suggesting that sequences distant from the transit sequence were brought into the vicinity of the outer membrane under these conditions. IAP75 and a third import component, IAP34, were coimmunoprecipitated with IAP86 antibodies from solubilized envelope membranes, indicating that these three proteins form a stable complex in the outer membrane. On the basis of these observations, we propose that IAP86 and IAP75 act as components of a multisubunit complex to mediate energy-independent recognition of the transit sequence and subsequent nucleoside triphosphate-induced insertion of the transit sequence across the outer membrane.
MeSH Terms
Animals
Biological Transport
Chloroplasts/metabolism
GTP-Binding Proteins/metabolism
Membrane Proteins/metabolism
Peas/metabolism
Peptides/metabolism
Plant Proteins
Protein Precursors/metabolism
Protein Sorting Signals/metabolism
Rabbits
Ribulose-Bisphosphate Carboxylase/metabolism
Chemicals
Membrane Proteins
OEP75 protein, Pisum sativum
Peptides
Plant Proteins
Protein Precursors
Protein Sorting Signals
GTP-Binding Proteins
Ribulose-Bisphosphate Carboxylase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ma Y
Department of Biological Sciences, Rutgers, State University of New Jersey, Newark 07102, USA.
Kouranov A
LaSala S E
Schnell D J
References (22)
22 references, click to expand
-
The binding of precursor proteins to chloroplasts requires nucleoside triphosphates in the intermembrane space.
J Biol Chem. 1992 Jan 5;267(1):433-9
PMID: 1730608
-
Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts.
Plant Physiol. 1984 Jul;75(3):675-8
PMID: 16663686
-
ATP is required for the binding of precursor proteins to chloroplasts.
J Biol Chem. 1989 Apr 25;264(12):6724-9
PMID: 2708339
-
Signal peptide analogs derived from two chloroplast precursors interact with the signal recognition system of the chloroplast envelope.
J Biol Chem. 1991 Feb 15;266(5):3335-42
PMID: 1993706
-
Protein import into chloroplasts requires a chloroplast ATPase.
Proc Natl Acad Sci U S A. 1987 May;84(10):3288-92
PMID: 2953027
-
Protein import into chloroplasts.
Trends Cell Biol. 1993 Jun;3(6):186-90
PMID: 14731492
-
Identification of intermediates in the pathway of protein import into chloroplasts and their localization to envelope contact sites.
J Cell Biol. 1993 Jan;120(1):103-15
PMID: 8416981
-
Copper chloride, an inhibitor of protein import into chloroplasts.
FEBS Lett. 1995 Jun 19;367(1):19-22
PMID: 7601278
-
Immunoprecipitation of proteins from cell-free translations.
Methods Enzymol. 1983;96:111-20
PMID: 6361451
-
Expression in Escherichia coli and purification of a translocation-competent precursor of the chloroplast protein ferredoxin.
J Biol Chem. 1990 Feb 25;265(6):3358-61
PMID: 2406251
-
Chloroplast protein import : quantitative analysis of precursor binding.
Plant Physiol. 1989 Mar;89(3):993-9
PMID: 16666654
-
A receptor component of the chloroplast protein translocation machinery.
Science. 1994 Dec 23;266(5193):1989-92
PMID: 7801125
-
Internal ATP is the only energy requirement for the translocation of precursor proteins across chloroplastic membranes.
J Biol Chem. 1989 Apr 25;264(12):6730-6
PMID: 2708340
-
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
-
Isolation of components of the chloroplast protein import machinery.
Science. 1994 Nov 11;266(5187):1007-12
PMID: 7973649
-
Precursors to two nuclear-encoded chloroplast proteins bind to the outer envelope membrane before being imported into chloroplasts.
J Biol Chem. 1985 Mar 25;260(6):3691-6
PMID: 3882712
-
Identification of chloroplast envelope proteins in close physical proximity to a partially translocated chimeric precursor protein.
J Biol Chem. 1994 Dec 23;269(51):32264-71
PMID: 7798226
-
A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway.
EMBO J. 1995 Jun 1;14(11):2436-46
PMID: 7781598
-
Identification of two GTP-binding proteins in the chloroplast protein import machinery.
Science. 1994 Nov 11;266(5187):1035-9
PMID: 7973656
-
Chloroplast protein topogenesis: import, sorting and assembly.
Biochim Biophys Acta. 1991 Nov 13;1071(3):221-53
PMID: 1958688
-
Envelope membrane proteins that interact with chloroplastic precursor proteins.
Plant Cell. 1994 Jan;6(1):93-105
PMID: 8130644
-
Shedding light on the chloroplast protein import machinery.
Cell. 1995 Nov 17;83(4):521-4
PMID: 7585953