Home LiteratureArticle Details
PMID: 15516497 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis.

Plant physiology ·Vol. 136 ·No. 3 ·2004-11-00 ·Pages 3605-15

Constan D, Froehlich JE, Rangarajan S, Keegstra K

Abstract

Molecular chaperones are required for the translocation of many proteins across organellar membranes, presumably by providing energy in the form of ATP hydrolysis for protein movement. In the chloroplast protein import system, a heat shock protein 100 (Hsp100), known as Hsp93, is hypothesized to be the chaperone providing energy for precursor translocation, although there is little direct evidence for this hypothesis. To learn more about the possible function of Hsp93 during protein import into chloroplasts, we isolated knockout mutant lines that contain T-DNA disruptions in either atHSP93-V or atHSP93-III, which encode the two Arabidopsis (Arabidopsis thaliana) homologs of Hsp93. atHsp93-V mutant plants are much smaller and paler than wild-type plants. In addition, mutant chloroplasts contain less thylakoid membrane when compared to the wild type. Plastid protein composition, however, seems to be largely unaffected in atHsp93-V knockout plants. Chloroplasts isolated from the atHsp93-V knockout mutant line are still able to import a variety of precursor proteins, but the rate of import of some of these precursors is significantly reduced. These results indicate that atHsp93-V has an important, but not essential, role in the biogenesis of Arabidopsis chloroplasts. In contrast, knockout mutant plants for atHsp93-III, the second Arabidopsis Hsp93 homolog, had a visible phenotype identical to the wild type, suggesting that atHsp93-III may not play as important a role as atHsp93-V in chloroplast development and/or function.

MeSH Terms
Arabidopsis/genetics,metabolism,ultrastructure Arabidopsis Proteins/metabolism,physiology Chlorophyll/metabolism Chloroplasts/genetics,metabolism,ultrastructure Gene Expression Regulation, Plant Heat-Shock Proteins/genetics,physiology Mutation Phenotype Plant Leaves/anatomy & histology,genetics Protein Transport/physiology Time Factors
Chemicals
Arabidopsis Proteins Heat-Shock Proteins Chlorophyll
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Constan Diane
Department of Energy Plant Research Laboratory , Michigan State University, East Lansing, Michigan 48824, USA.
Froehlich John E
Rangarajan Sowkya
Keegstra Kenneth
References (49)
49 references, click to expand
  1. ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis.
    Mol Microbiol. 1999 May;32(3):581-93 PMID: 10320580
  2. Identification of clp genes expressed in senescing Arabidopsis leaves.
    Plant Cell Physiol. 1999 May;40(5):504-14 PMID: 10427773
  3. COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS.
    Plant Physiol. 1949 Jan;24(1):1-15 PMID: 16654194
  4. HSP104 required for induced thermotolerance.
    Science. 1990 Jun 1;248(4959):1112-5 PMID: 2188365
  5. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  6. The mitochondrial protein import motor.
    Biol Chem. 2000 Sep-Oct;381(9-10):943-9 PMID: 11076025
  7. Toc, tic, and chloroplast protein import.
    Biochim Biophys Acta. 2002 Jun 12;1590(1-3):177-89 PMID: 12180471
  8. Escherichia coli contains a soluble ATP-dependent protease (Ti) distinct from protease La.
    Proc Natl Acad Sci U S A. 1987 Aug;84(16):5550-4 PMID: 3303028
  9. The ClpX heat-shock protein of Escherichia coli, the ATP-dependent substrate specificity component of the ClpP-ClpX protease, is a novel molecular chaperone.
    EMBO J. 1995 May 1;14(9):1867-77 PMID: 7743994
  10. Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking.
    J Cell Biol. 1997 Mar 10;136(5):983-94 PMID: 9060464
  11. A nuclear-coded chloroplastic inner envelope membrane protein uses a soluble sorting intermediate upon import into the organelle.
    J Cell Biol. 1997 Jun 16;137(6):1279-86 PMID: 9182662
  12. Protein translocation: how Hsp70 pulls it off.
    Cell. 1999 Jun 11;97(6):679-82 PMID: 10380919
  13. A new component of bacteriophage Mu replicative transposition machinery: the Escherichia coli ClpX protein.
    Mol Microbiol. 1994 Mar;11(6):1109-16 PMID: 8022280
  14. The cyanobacterium Synechococcus sp. PCC 7942 possesses a close homologue to the chloroplast ClpC protein of higher plants.
    Plant Mol Biol. 1996 Jul;31(4):721-30 PMID: 8806403
  15. Protein import into chloroplasts.
    Trends Cell Biol. 1999 Jun;9(6):222-7 PMID: 10354568
  16. A molecular chaperone, ClpA, functions like DnaK and DnaJ.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12218-22 PMID: 7991609
  17. Full-length plastocyanin precursor is translocated across isolated thylakoid membranes.
    J Biol Chem. 1991 Mar 25;266(9):5876-83 PMID: 2005123
  18. HSP100/Clp proteins: a common mechanism explains diverse functions.
    Trends Biochem Sci. 1996 Aug;21(8):289-96 PMID: 8772382
  19. A high-throughput Arabidopsis reverse genetics system.
    Plant Cell. 2002 Dec;14(12):2985-94 PMID: 12468722
  20. A nuclear gene, erd1, encoding a chloroplast-targeted Clp protease regulatory subunit homolog is not only induced by water stress but also developmentally up-regulated during senescence in Arabidopsis thaliana.
    Plant J. 1997 Oct;12(4):851-61 PMID: 9375397
  21. Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport.
    Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):8145-50 PMID: 8755618
  22. A regulatory switch involving a Clp ATPase.
    Bioessays. 1997 Jun;19(6):455-8 PMID: 9204762
  23. Molecular chaperones as essential mediators of mitochondrial biogenesis.
    Biochim Biophys Acta. 2002 Sep 2;1592(1):51-62 PMID: 12191768
  24. Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon.
    EMBO J. 2003 Jun 16;22(12):2970-80 PMID: 12805212
  25. 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
  26. ClpB is the Escherichia coli heat shock protein F84.1.
    J Bacteriol. 1991 Jul;173(14):4254-62 PMID: 2066329
  27. Protein translocation: is Hsp70 pulling my chain?
    Curr Biol. 1999 Oct 21;9(20):R779-82 PMID: 10531024
  28. Mutations in ClpC2/Hsp100 suppress the requirement for FtsH in thylakoid membrane biogenesis.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12765-70 PMID: 15304652
  29. The two-component, ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component.
    J Biol Chem. 1988 Oct 15;263(29):15226-36 PMID: 3049606
  30. Isolation of components of the chloroplast protein import machinery.
    Science. 1994 Nov 11;266(5187):1007-12 PMID: 7973649
  31. Chloroplast division and morphology are differentially affected by overexpression of FtsZ1 and FtsZ2 genes in Arabidopsis.
    Plant Physiol. 2000 Dec;124(4):1668-77 PMID: 11115884
  32. Characterization of Chloroplast Clp proteins in Arabidopsis: Localization, tissue specificity and stress responses.
    Physiol Plant. 2002 Jan;114(1):92-101 PMID: 11982939
  33. Characterization of a cDNA clone encoding a chloroplast-targeted Clp homologue.
    Plant Mol Biol. 1993 Feb;21(3):525-37 PMID: 8443344
  34. Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance.
    J Bacteriol. 1994 Jun;176(11):3360-7 PMID: 8195092
  35. Travelling of proteins through membranes: translocation into chloroplasts.
    Planta. 2000 Sep;211(4):449-56 PMID: 11030543
  36. 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
  37. Cytochrome P450-dependent metabolism of oxylipins in tomato. Cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase.
    Plant Physiol. 2000 Jun;123(2):711-24 PMID: 10859201
  38. Protein import and routing systems of chloroplasts.
    Plant Cell. 1999 Apr;11(4):557-70 PMID: 10213778
  39. Molecular chaperones and protein folding in plants.
    Plant Mol Biol. 1996 Oct;32(1-2):191-222 PMID: 8980480
  40. Posttranslational protein translocation across the membrane of the endoplasmic reticulum.
    Biol Chem. 1999 Oct;380(10):1143-50 PMID: 10595576
  41. Protein transport into mitochondria.
    Curr Opin Microbiol. 2000 Apr;3(2):210-4 PMID: 10744987
  42. Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone.
    EMBO J. 1997 Mar 3;16(5):935-46 PMID: 9118955
  43. The stroma of higher plant plastids contain ClpP and ClpC, functional homologs of Escherichia coli ClpP and ClpA: an archetypal two-component ATP-dependent protease.
    Plant Cell. 1995 Oct;7(10):1713-22 PMID: 7580259
  44. A method for isolating a high yield of Arabidopsis chloroplasts capable of efficient import of precursor proteins.
    Plant J. 2001 Jul;27(1):59-65 PMID: 11489183
  45. T-DNA as an insertional mutagen in Arabidopsis.
    Plant Cell. 1999 Dec;11(12):2283-90 PMID: 10590158
  46. Mitochondrial preprotein translocase.
    Annu Rev Cell Dev Biol. 1997;13:25-51 PMID: 9442867
  47. Effects of light and temperature on expression of ClpC, the regulatory subunit of chloroplastic Clp protease, in pea seedlings.
    Plant Mol Biol. 1996 Jun;31(3):673-6 PMID: 8790298
  48. Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane.
    J Cell Biol. 1998 Nov 16;143(4):991-1002 PMID: 9817756
  49. Precursors with altered affinity for Hsp70 in their transit peptides are efficiently imported into chloroplasts.
    J Biol Chem. 2003 Nov 21;278(47):46473-81 PMID: 12970339
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2004-11-00
Epub
2004-00-29
Pages
3605-15
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC527159
Subset
IM
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: [email protected]