Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes

Plant Physiology

Volumn 141, Issue 1, 2006, Pages 47-60

  Changle, Ma ^a   Haslbeck, Martin ^b   Babujee, Lavanya ^a,d   Jahn, Olaf ^c   Reumann, Sigrun ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^d SHIZUOKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTROPHORESIS; ENZYMES; FLUORESCENCE; GENES; PROTEINS;

FLUORESCENT PROTEIN; FUSION PROTEINS; HEAT-SHOCK PROTEINS (SHSP); PEROXISOMAL LOCALIZATION;

PLANTS (BOTANY);

ENZYMES; GENES; PLANTS; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 33745451171     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.105.073841     Document Type: Article

References (53)

1. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815
2. Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24: 1-15
3. Banzet N, Richaud C, Deveaux Y, Kazmaier M, Gagnon J, Triantaphylides C (1998) Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. Plant J 13: 519-527
4. Beevers H (1979) Microbodies in higher plants. Annu Rev Plant Physiol 30: 159-193
5. Buchner J, Grallert H, Jakob U (1998) Analysis of chaperone function using citrate synthase as a nonnative substrate protein. Methods Enzymol 290: 323-338
6. Cashikar AG, Duennwald M, Lindquist SL (2005) A chaperone pathway in protein disaggregation: Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J Biol Chem 280: 23869-23875
7. Chandler JW, Melzer S (2004) An alpha-crystallin gene, ACD31.2 from Arabidopsis is negatively regulated by FPF1 overexpression, floral induction, gibberellins, and long days. J Exp Bot 55: 1433-1435
8. De Jong WW, Caspers GJ, Leunissen JA (1998) Genealogy of the alpha-crystallin-small heat-shock protein superfamily. Int J Biol Macromol 22: 151-162
9. del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53: 1255-1272
10. Diefenbach J, Kindl H (2000) The membrane-bound DnaJ protein located at the cytosolic site of glyoxysomes specifically binds the cytosolic isoform 1 of Hsp70 but not other Hsp70 species. Eur J Biochem 267: 746-754
11. Feierabend J, Engel S (1986) Photoinactivation of catalase in vitro and in leaves. Arch Biochem Biophys 251: 567-576
12. Forreiter C, Kirschner M, Nover L (1997) Stable transformation of an Arabidopsis cell suspension culture with firefly luciferase providing a cellular system for analysis of chaperone activity in vivo. Plant Cell 9: 2171-2181
13. Fukao Y, Hayashi M, Hara-Nishimura I, Nishimura M (2003) Novel glyoxysomal protein kinase, GPK1, identified by proteomic analysis of glyoxysomes in etiolated cotyledons of Arabidopsis thaliana. Plant Cell Physiol 44: 1002-1012
14. Fukao Y, Hayashi M, Nishimura M (2002) Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant Cell Physiol 43: 689-696
15. Fulda M, Shockey J, Werber M, Wolter FP, Heinz E (2002) Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid beta-oxidation. Plant J 32: 93-103
16. Gobom J, Schuerenberg M, Mueller M, Theiss D, Lehrach H, Nordhoff E (2001) Alpha-cyano-4-hydroxycinnamic acid affinity sample preparation: a protocol for MALDI-MS peptide analysis in proteomics. Anal Chem 73: 434-438
17. Grotjohann N, Janning A, Eising R (1997) In vitro photoinactivation of catalase isoforms from cotyledons of sunflower (Helianthus annuus L.). Arch Biochem Biophys 346: 208-218
18. Härndahl U, Hall RB, Osteryoung KW, Vierling E, Bornman JF, Sundby C (1999) The chloroplast small heat shock protein undergoes oxidation-dependent conformational changes and may protect plants from oxidative stress. Cell Stress Chaperones 4: 129-138
19. Haslbeck M, Braun N, Stromer T, Richter B, Model N, Weinkauf S, Buchner J (2004) Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J 23: 638-649
20. Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12: 842-846
21. Haslbeck M, Walke S, Stromer T, Ehrnsperger M, White HE, Chen S, Saibil HR, Buchner J (1999) Hsp26: a temperature-regulated chaperone. EMBO J 18: 6744-6751
22. Johnson TL, Olsen LJ (2001) Building new models for peroxisome biogenesis. Plant Physiol 127: 731-739
23. Kamigaki A, Mano S, Terauchi K, Nishi Y, Tachibe-Kinoshita Y, Nito K, Kondo M, Hayashi M, Nishimura M, Esaka M (2003) Identification of peroxisomal targeting signal of pumpkin catalase and the binding analysis with PTS1 receptor. Plant J 33: 161-175
24. Kato A, Takeda-Yoshikawa Y, Hayashi M, Kondo M, Hara-Nishimura I, Nishimura M (1998) Glyoxysomal malate dehydrogenase in pumpkin: cloning of a cDNA and functional analysis of its presequence. Plant Cell Physiol 39: 186-195
25. Lee GJ (1995) Assaying proteins for molecular chaperone activity. Methods Cell Biol 50: 325-334
26. Lee GJ, Vierling E (2000) A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol 122: 189-198
27. Lee JH, Hubel A, Schoffl F (1995) Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased hermotolerance in transgenic Arabidopsis. Plant J 8: 603-612
28. Lisenbee CS, Lingard MJ, Trelease RN (2005) Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J 43: 900-914
29. Lopez-Huertas E, Charlton WL, Johnson B, Graham IA, Baker A (2000) Stress induces peroxisome biogenesis genes. EMBO J 19: 6770-6777
30. Low D, Brandle K, Nover L, Forreiter C (2000) Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta 211: 575-582
31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Polin phenol reagent. J Biol Chem 193: 265-275
32. Mogk A, Deuerling E, Vorderwulbecke S, Vierling E, Bukau B (2003) Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol 50: 585-595
33. Narberhaus F (2002) Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66: 64-93
34. Neuberger G, Kunze M, Eisenhaber F, Berger J, Hartig A, Brocard C (2004) Hidden localization motifs: naturally occurring peroxisomal targeting signals in non-peroxisomal proteins. Genome Biol 5: R97
35. Petko L, Lindquist S (1986) Hsp26 is not required for growth at high temperatures, nor for thermotolerance, spore development, or germination. Cell 45: 885-894
36. Reumann S (2002) The photorespiratory pathway of leaf peroxisomes. In A Baker, IA Graham, eds, Plant Peroxisomes: Biochemistry, Cell Biology and Biotechnological Applications, Ed 1. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 141-189
37. Reumann S (2004) Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol 135: 783-800
38. Reumann S, Ma C, Lemke S, Babujee L (2004) AraPerox: a database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiol 136: 2587-2608
39. Reumann S, Maier E, Benz R, Heldt HW (1995) The membrane of leaf peroxisomes contains a porin-like channel. J Biol Chem 270: 17559-17565
40. Scharf KD, Siddique M, Vierling E (2001) The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing alpha-crystallin domains (Acd proteins). Cell Stress Chaperones 6: 225-237
41. Sharkey T (1988) Estimating the rate of photorespiration in leaves. Physiol Plant 73: 147-152
42. Spector DL, Goldmann RD, Leinwand LA (1998) Preparative methods for scanning electron microscopy. In DL Spector, RD Goldmann, LA Leinwand, eds, Cells. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 122.1-123.27
43. Suckau D, Resemann A, Schuerenberg M, Hufnagel P, Franzen J, Holle A (2003) A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics. Anal Bioanal Chem 376: 952-965
44. Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577: 1-9
45. van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8: 1025-1030
46. Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42: 579-620
47. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9: 244-252
48. Wessel D, Flügge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138: 141-143
49. Wimmer B, Lottspeich F, van der Klei I, Veenhuis M, Gietl C (1997) The glyoxysomal and plastid molecular chaperones (70-kDa heat shock protein) of watermelon cotyledons are encoded by a single gene. Proc Natl Acad Sci USA 94: 13624-13629
50. Wotton D, Freeman K, Shore D (1996) Multimerization of Hsp42p, a novel heat shock protein of Saccharomyces cerevisiae, is dependent on a conserved carboxyl-terminal sequence. J Biol Chem 271: 2717-2723
51. Young JC, Barral JM, Hartl UF (2003) More than folding: localized functions of cytosolic chaperones. Trends Biochem Sci 28: 541-547
52. Yu C, Huang AH (1986) Conversion of serine to glycerate in intact spinach leaf peroxisomes: role of malate dehydrogenase. Arch Biochem Biophys 245: 125-133
53. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621-2632