Home LiteratureArticle Details
PMID: 9636172 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

A chloroplast processing enzyme functions as the general stromal processing peptidase.

Richter S, Lamppa GK

Abstract

A highly specific stromal processing activity is thought to cleave a large diversity of precursors targeted to the chloroplast, removing an N-terminal transit peptide. The identity of this key component of the import machinery has not been unequivocally established. We have previously characterized a chloroplast processing enzyme (CPE) that cleaves the precursor of the light-harvesting chlorophyll a/b binding protein of photosystem II (LHCPII). Here we report the overexpression of active CPE in Escherichia coli. Examination of the recombinant enzyme in vitro revealed that it cleaves not only preLHCPII, but also the precursors for an array of proteins essential for different reactions and destined for different compartments of the organelle. CPE also processes its own precursor in trans. Neither the recombinant CPE nor the native CPE of chloroplasts process a preLHCPII mutant with an altered cleavage site demonstrating that both forms of the enzyme are sensitive to the same structural modification of the substrate. The transit peptide of the precursor of ferredoxin is released by a single cleavage event and found intact after processing by recombinant CPE and a chloroplast extract as well. These results provide the first direct demonstration that CPE is the general stromal processing peptidase that acts as an endopeptidase. Significantly, recombinant CPE cleaves in the absence of other chloroplast proteins, and this activity depends on metal cations, such as zinc.

MeSH Terms
Amino Acid Sequence Apoproteins/metabolism Arabidopsis Arabidopsis Proteins Chloroplasts/enzymology Escherichia coli Light-Harvesting Protein Complexes Metalloendopeptidases/metabolism Metals/metabolism Molecular Sequence Data Photosynthetic Reaction Center Complex Proteins/metabolism Photosystem II Protein Complex Plant Proteins Protein Precursors/metabolism Protein Processing, Post-Translational Recombinant Proteins/metabolism Sequence Alignment
Chemicals
Apoproteins Arabidopsis Proteins Light-Harvesting Protein Complexes Metals Photosynthetic Reaction Center Complex Proteins Photosystem II Protein Complex Plant Proteins Protein Precursors Recombinant Proteins Metalloendopeptidases chloroplast processing enzyme protein, Arabidopsis stromal processing peptidase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Richter S
Department of Molecular Genetics and Cell Biology, University of Chicago, 920 E. 58th Street, Chicago, IL 60637, USA.
Lamppa G K
References (44)
44 references, click to expand
  1. Characterization and subcellular localization of aminopeptidases in senescing barley leaves.
    Plant Physiol. 1988;87:894-7 PMID: 11537879
  2. Mechanism of Protein Transport across the Chloroplast Envelope.
    Plant Physiol. 1997 Jun;114(2):405-410 PMID: 12223715
  3. HD-Zip proteins: members of an Arabidopsis homeodomain protein superfamily.
    Proc Natl Acad Sci U S A. 1992 May 1;89(9):3894-8 PMID: 1349174
  4. Identification of two structurally related proteins involved in proteolytic processing of precursors targeted to the chloroplast.
    EMBO J. 1992 Dec;11(12):4401-9 PMID: 1385116
  5. Biophysical characterization of a transit peptide directing chloroplast protein import.
    Biochemistry. 1992 Jun 2;31(21):5053-60 PMID: 1534691
  6. Properties of a Chloroplast Enzyme that Cleaves the Chlorophyll a/b Binding Protein Precursor : Optimization of an Organelle-Free Reaction.
    Plant Physiol. 1989 May;90(1):117-24 PMID: 16666720
  7. Soluble Chloroplast Enzyme Cleaves preLHCP Made in Escherichia coli to a Mature Form Lacking a Basic N-Terminal Domain.
    Plant Physiol. 1991 Aug;96(4):1220-7 PMID: 16668323
  8. Processing of the Precursors for the Light-Harvesting Chlorophyll-Binding Proteins of Photosystem II and Photosystem I during Import and in an Organelle-Free Assay.
    Plant Physiol. 1992 Feb;98(2):595-601 PMID: 16668683
  9. Differential induction of 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase genes in Arabidopsis thaliana by wounding and pathogenic attack.
    Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8821-5 PMID: 1681544
  10. Transport of proteins into chloroplasts. Delineation of envelope "transit" and thylakoid "transfer" signals within the pre-sequences of three imported thylakoid lumen proteins.
    J Biol Chem. 1991 Dec 15;266(35):23606-10 PMID: 1748638
  11. Nucleotide sequence of a cDNA clone encoding the precursor of the 33 kDa protein of the oxygen-evolving complex from wheat.
    Plant Mol Biol. 1991 Jun;16(6):1085-7 PMID: 1863762
  12. Nucleotide sequence of cDNA encoding the precursor of the 23 kDa protein of the photosynthetic oxygen-evolving complex from wheat.
    Plant Mol Biol. 1991 Jul;17(1):179-82 PMID: 1868221
  13. Determinants for cleavage of the chlorophyll a/b binding protein precursor: a requirement for a basic residue that is not universal for chloroplast imported proteins.
    J Cell Biol. 1991 Aug;114(4):681-8 PMID: 1869585
  14. Chloroplast transit peptides. The perfect random coil?
    FEBS Lett. 1991 Jan 14;278(1):1-3 PMID: 1993469
  15. The gamma-subunit of spinach chloroplast ATP synthase: isolation and characterisation of cDNA and genomic clones.
    Plant Mol Biol. 1990 Jun;14(6):1007-18 PMID: 2151716
  16. Use of T7 RNA polymerase to direct expression of cloned genes.
    Methods Enzymol. 1990;185:60-89 PMID: 2199796
  17. A conserved cleavage-site motif in chloroplast transit peptides.
    FEBS Lett. 1990 Feb 26;261(2):455-8 PMID: 2311769
  18. Isolation of a cDNA clone for the acyl carrier protein-I of spinach.
    Plant Mol Biol. 1987 Mar;9(2):127-34 PMID: 24276902
  19. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa.
    Anal Biochem. 1987 Nov 1;166(2):368-79 PMID: 2449095
  20. Targeting of proteins to the thylakoid lumen by the bipartite transit peptide of the 33 kd oxygen-evolving protein.
    EMBO J. 1989 Nov;8(11):3187-94 PMID: 2583096
  21. Transport of proteins into chloroplasts. Import and maturation of precursors to the 33-, 23-, and 16-kDa proteins of the photosynthetic oxygen-evolving complex.
    J Biol Chem. 1989 Nov 25;264(33):19573-6 PMID: 2684958
  22. A thylakoid processing protease is required for complete maturation of the lumen protein plastocyanin.
    Nature. 1986 Dec 11;324(6097):567-569 PMID: 29517759
  23. The plant ferredoxin precursor: nucleotide sequence of a full length cDNA clone.
    Nucleic Acids Res. 1985 May 10;13(9):3179-94 PMID: 2987875
  24. Structure and expression of spinach leaf cDNA encoding ribulosebisphosphate carboxylase/oxygenase activase.
    Proc Natl Acad Sci U S A. 1988 Feb;85(3):787-91 PMID: 3277181
  25. Processing of a wheat light-harvesting chlorophyll a/b protein precursor by a soluble enzyme from higher plant chloroplasts.
    J Cell Biol. 1987 Dec;105(6 Pt 1):2641-8 PMID: 3320051
  26. A cDNA clone encoding a photosystem I protein with homology to photosystem II chlorophyll a/b-binding polypeptides.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):8844-8 PMID: 3321058
  27. A heat shock protein localized to chloroplasts is a member of a eukaryotic superfamily of heat shock proteins.
    EMBO J. 1988 Mar;7(3):575-81 PMID: 3396532
  28. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes.
    J Biol Chem. 1987 Jul 25;262(21):10035-8 PMID: 3611052
  29. Structure and developmental regulation of a wheat gene encoding the major chlorophyll a/b-binding polypeptide.
    Mol Cell Biol. 1985 Jun;5(6):1370-8 PMID: 3897835
  30. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  31. Transport of proteins into chloroplasts. Partial purification of a chloroplast protease involved in the processing of important precursor polypeptides.
    Eur J Biochem. 1984 Jul 16;142(2):337-42 PMID: 6430703
  32. Tissue-specific and light-regulated expression of a pea nuclear gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase.
    EMBO J. 1984 Aug;3(8):1671-9 PMID: 6479146
  33. A comprehensive set of sequence analysis programs for the VAX.
    Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95 PMID: 6546423
  34. Establishing homologies in protein sequences.
    Methods Enzymol. 1983;91:524-45 PMID: 6855599
  35. A chloroplast processing enzyme involved in precursor maturation shares a zinc-binding motif with a recently recognized family of metalloendopeptidases.
    Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7177-81 PMID: 7638164
  36. Mutations at the stromal processing peptidase cleavage site of a thylakoid lumen protein precursor affect the rate of processing but not the fidelity.
    J Biol Chem. 1994 Jun 10;269(23):16062-6 PMID: 8206905
  37. Analysis of chloroplast transit peptide function using mutations in the carboxyl-terminal region.
    Plant Mol Biol. 1993 Dec;23(6):1105-15 PMID: 8292776
  38. A role in DNA binding for the linker sequences of the first three zinc fingers of TFIIIA.
    Nucleic Acids Res. 1993 Jul 25;21(15):3341-6 PMID: 8346014
  39. Evolutionary families of peptidases.
    Biochem J. 1993 Feb 15;290 ( Pt 1):205-18 PMID: 8439290
  40. Identification of interdomain sequences promoting the intronless evolution of a bacterial protein family.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8490-5 PMID: 8710897
  41. Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information.
    Nucleic Acids Res. 1996 Sep 1;24(17):3439-52 PMID: 8811101
  42. Import and routing of nucleus-encoded chloroplast proteins.
    Annu Rev Cell Dev Biol. 1996;12:1-26 PMID: 8970720
  43. Seventy-five percent accuracy in protein secondary structure prediction.
    Proteins. 1997 Mar;27(3):329-35 PMID: 9094735
  44. Unique organization of the dnaA region from Prochlorococcus marinus CCMP1375, a marine cyanobacterium.
    Mol Gen Genet. 1998 Mar;257(5):534-41 PMID: 9563839
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1998-06-23
Pages
7463-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC22651
Subset
IM
Databases
GENBANK
AF008444
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com