Home LiteratureArticle Details
PMID: 15879560 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation.

The Plant cell ·Vol. 17 ·No. 6 ·2005-06-00 ·Pages 1829-38

Neta-Sharir I, Isaacson T, Lurie S, Weiss D

Abstract

The tomato (Lycopersicon esculentum) chloroplast small heat shock protein (sHSP), HSP21, is induced by heat treatment in leaves, but also under normal growth conditions in developing fruits during the transition of chloroplasts to chromoplasts. We used transgenic tomato plants constitutively expressing HSP21 to study the role of the protein under stress conditions and during fruit maturation. Although we did not find any effect for the transgene on photosystem II (PSII) thermotolerance, our results show that the protein protects PSII from temperature-dependent oxidative stress. In addition, we found direct evidence of the protein's role in fruit reddening and the conversion of chloroplasts to chromoplasts. When plants were grown under normal growth temperature, transgenic fruits accumulated carotenoids earlier than controls. Furthermore, when detached mature green fruits were stored for 2 weeks at 2 degrees C and then transferred to room temperature, the natural accumulation of carotenoids was blocked. In a previous study, we showed that preheat treatment, which induces HSP21, allowed fruit color change at room temperature, after a cold treatment. Here, we show that mature green transgenic fruits constitutively expressing HSP21 do not require the heat treatment to maintain the ability to accumulate carotenoids after cold storage. This study demonstrates that a sHSP plays a role in plant development under normal growth conditions, in addition to its protective effect under stress conditions.

MeSH Terms
Arabidopsis Proteins/genetics Carotenoids/metabolism Chloroplasts/genetics,metabolism Fruit/genetics,growth & development,metabolism Heat-Shock Proteins/genetics,metabolism Lycopersicon esculentum/genetics,growth & development,metabolism Molecular Sequence Data Oxidative Stress/physiology Photosystem II Protein Complex/genetics,metabolism Plant Proteins/metabolism Plants, Genetically Modified/genetics,growth & development,metabolism Plastids/genetics,metabolism Temperature
Chemicals
Arabidopsis Proteins HSP21 protein, Arabidopsis Heat-Shock Proteins Photosystem II Protein Complex Plant Proteins Carotenoids
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Neta-Sharir Inbal
Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agricultural, Food, and Environmental Quality Sciences, Hebrew University of Jerusalem, Rehovot 76100, Israel.
Isaacson Tal
Lurie Susan
Weiss David
References (37)
37 references, click to expand
  1. Abundance of the Major Chloroplast Polypeptides during Development and Ripening of Tomato Fruits: An Immunological Study.
    Plant Physiol. 1988 May;87(1):239-43 PMID: 16666110
  2. Cloning of the two chalcone flavanone isomerase genes from Petunia hybrida: coordinate, light-regulated and differential expression of flavonoid genes.
    EMBO J. 1988 May;7(5):1257-63 PMID: 3409864
  3. Maintenance of Chloroplast Components during Chromoplast Differentiation in the Tomato Mutant Green Flesh.
    Plant Physiol. 1993 Apr;101(4):1223-1229 PMID: 12231777
  4. Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo.
    Planta. 2000 Sep;211(4):575-82 PMID: 11030557
  5. Cloning and characterization of the cDNA for lycopene beta-cyclase from tomato reveals decrease in its expression during fruit ripening.
    Plant Mol Biol. 1996 Feb;30(4):807-19 PMID: 8624411
  6. Synthesis of small heat-shock proteins is part of the developmental program of late seed maturation.
    Plant Physiol. 1996 Oct;112(2):747-57 PMID: 8883386
  7. Dual regulation of a heat shock promoter during embryogenesis: stage-dependent role of heat shock elements.
    Plant J. 1998 Feb;13(4):437-46 PMID: 9680992
  8. Expression of plant genes in transfected mammalian cells: accumulation of recombinant preLHCIIb proteins within cytoplasmic inclusion bodies.
    Exp Cell Res. 1991 Jan;192(1):248-55 PMID: 1984416
  9. Cloning and molecular characterization of a strawberry fruit ripening-related cDNA corresponding a mRNA for a low-molecular-weight heat-shock protein.
    Plant Mol Biol. 1998 Jan;36(1):33-42 PMID: 9484460
  10. Cysteine synthase from Capsicum annuum chromoplasts. Characterization and cDNA cloning of an up-regulated enzyme during fruit development.
    J Biol Chem. 1992 Sep 5;267(25):17966-70 PMID: 1381358
  11. Analysis in vitro of the enzyme CRTISO establishes a poly-cis-carotenoid biosynthesis pathway in plants.
    Plant Physiol. 2004 Dec;136(4):4246-55 PMID: 15557094
  12. Novel and useful properties of a chimeric plant promoter combining CaMV 35S and MAS elements.
    Plant Mol Biol. 1990 Sep;15(3):373-81 PMID: 2103458
  13. Impacts of chilling temperatures on photosynthesis in warm-climate plants.
    Trends Plant Sci. 2001 Jan;6(1):36-42 PMID: 11164376
  14. Dynamics of small heat shock protein distribution within the chloroplasts of higher plants.
    J Biol Chem. 1994 Nov 18;269(46):28676-82 PMID: 7961818
  15. Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis.
    Plant Physiol. 1986 Jul;81(3):802-6 PMID: 16664906
  16. Chromoplast development in ripening tomato fruit: identification of cDNAs for chromoplast-targeted proteins and characterization of a cDNA encoding a plastid-localized low-molecular-weight heat shock protein.
    Plant Mol Biol. 1997 Feb;33(3):483-92 PMID: 9049268
  17. Heat sensitivity in a bentgrass variant. Failure to accumulate a chloroplast heat shock protein isoform implicated in heat tolerance.
    Plant Physiol. 2003 Sep;133(1):319-27 PMID: 12970497
  18. Small heat-shock proteins regulate membrane lipid polymorphism.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13504-9 PMID: 12368478
  19. Small heat shock proteins and stress tolerance in plants.
    Biochim Biophys Acta. 2002 Aug 19;1577(1):1-9 PMID: 12151089
  20. The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress.
    Plant Physiol. 1998 Jan;116(1):439-444 PMID: 9449851
  21. A peptide methionine sulfoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein.
    Plant J. 2002 Mar;29(5):545-53 PMID: 11874568
  22. The chloroplast small heat shock protein undergoes oxidation-dependent conformational changes and may protect plants from oxidative stress.
    Cell Stress Chaperones. 1999 Jun;4(2):129-38 PMID: 10547062
  23. At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression.
    Plant J. 2001 Sep;27(5):407-15 PMID: 11576425
  24. Expression of small heat-shock proteins at low temperatures. A possible role in protecting against chilling injuries.
    Plant Physiol. 1998 Jun;117(2):651-8 PMID: 9625718
  25. The chaperone-like activity of a small heat shock protein is lost after sulfoxidation of conserved methionines in a surface-exposed amphipathic alpha-helix.
    Biochim Biophys Acta. 2001 Feb 9;1545(1-2):227-37 PMID: 11342048
  26. The correlation between heat-shock protein accumulation and persistence and chilling tolerance in tomato fruit.
    Plant Physiol. 1996 Feb;110(2):531-7 PMID: 8742333
  27. Methionine residues as endogenous antioxidants in proteins.
    Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15036-40 PMID: 8986759
  28. A 10-kDa class-CI sHsp protects E. coli from oxidative and high-temperature stress.
    Planta. 2003 Sep;217(5):813-9 PMID: 12743825
  29. Analysis of conserved domains identifies a unique structural feature of a chloroplast heat shock protein.
    Mol Gen Genet. 1991 May;226(3):425-31 PMID: 2038305
  30. Does the chloroplast small heat shock protein protect photosystem II during heat stress in vitro?
    Physiol Plant. 2001 Mar;111(3):273-275 PMID: 11240909
  31. A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state.
    EMBO J. 1997 Feb 3;16(3):659-71 PMID: 9034347
  32. Regulation of carotenoid biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta.
    Plant J. 1999 Feb;17(4):341-51 PMID: 10205893
  33. Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine.
    Plant Physiol. 2001 Jul;126(3):1266-74 PMID: 11457977
  34. Fruits: A Developmental Perspective.
    Plant Cell. 1993 Oct;5(10):1439-1451 PMID: 12271039
  35. Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin.
    Proc Natl Acad Sci U S A. 1982 Apr;79(7):2360-4 PMID: 6285380
  36. A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein.
    Plant Physiol. 2000 Jan;122(1):189-98 PMID: 10631262
  37. Substitution of conserved methionines by leucines in chloroplast small heat shock protein results in loss of redox-response but retained chaperone-like activity.
    Protein Sci. 2001 Sep;10(9):1785-93 PMID: 11514669
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2005-06-00
Epub
2005-00-06
Pages
1829-38
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1143080
Subset
IM
Databases
GENBANK
U66300
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