Nitric oxide and reactive oxygen species regulate the accumulation of heat shock proteins in tomato leaves in response to heat shock and pathogen infection

Plant Science

Volumn 207, Issue , 2013, Pages 57-65

  Piterková, Jana ^a   Luhová, Lenka ^a   Mieslerová, Barbora ^a   Lebeda, AleŠ ^a   Petřivalský, Marek ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

Heat shock proteins; Nitric oxide; Oidium neolycopersici; Reactive oxygen species; Solanum spp.; Tomato

Indexed keywords

HEAT SHOCK PROTEIN 70; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE;

ARTICLE; ASCOMYCETES; GENETICS; HEAT SHOCK RESPONSE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; SOLANUM; TOMATO;

ASCOMYCOTA; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; LYCOPERSICON ESCULENTUM; NITRIC OXIDE; PLANT DISEASES; REACTIVE OXYGEN SPECIES; SOLANUM;

EID: 84875090152     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2013.02.010     Document Type: Article

References (53)

1. Fu S., Meeley R., Scanlon M.J. Empty pericarp2 encodes a negative regulator of the heat shock response and is required for maize embryogenesis. Plant Cell 2002, 14:3119-3132.
2. Vierling E. The roles of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991, 42:579-620.
3. Morimoto R.I., Sarge K.D., Abravaya K. Transcriptional regulation of heat shock genes. A paradigm for inducible genomic responses. J. Biol. Chem. 1992, 267:21987-21990.
4. Iba K. Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu. Rev. Plant Biol. 2002, 53:225-245.
5. Wang W., Vinocur B., Shoseyov O., Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 2004, 9:244-252.
6. Frydman J. Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu. Rev. Biochem. 2001, 70:603-647.
7. Zhang X.-P., Glaser E. Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci. 2002, 7:14-21.
8. Scharf K.-D., Heider H., Höhfeld I., Lyck R., Schmidt E., Nover L. The tomato Hsf system: hsfa2 needs interaction with hsfa1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol. Cell. Biol. 1998, 18:2240-2251.
9. Mishra S.K., Tripp J., Winkelhaus S., Tschiersch B., Theres K., Nover L., Scharf K.-D. In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 2002, 16:1555-1567.
10. Hahn A., Bublak D., Schleiff E., Scharf K.-D. Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 2011, 23:741-755.
11. Gould K.S., Lamotte O., Klinguer A., Pugin A., Wendehenne D. Nitric oxide production in tobacco leaf cells: a generalized stress response?. Plant Cell Environ. 2003, 26:1851-1862.
12. Neill S.J., Desikan R., Clarke A., Hurst R.D., Hancock J.T. Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 2002, 53:1237-1247.
13. Mur L.A., Carver T.L., Prats E. NO way to live; the various roles of nitric oxide in plant-pathogen interactions. J. Exp. Bot. 2006, 57:489-505.
14. Song L., Ding W., Zhao M., Sun B., Zhang L. Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci. 2006, 171:449-458.
15. Ahn S.-G., Thiele D.J. Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev. 2003, 17:516-528.
16. Larkindale J., Knight M.R. Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 2002, 128:682-695.
17. Vacca R.A., de Pinto M.C., Valenti D., Passarella S., Marra E., De Gara L. Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells. Plant Physiol. 2004, 134:1100-1112.
18. Mittler R., Vanderauwera S., Gollery M., Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004, 9:490-498.
19. Uchida A., Jagendorf A., Hibino T., Takabe T., Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 2002, 163:515-523.
20. Corpas F.J., Chaki M., Fernandez-Ocana A., Valderrama R., Palma J.M., Carreras A., Begara-Morales J.C., Airaki M., del Rio L.A., Barroso J.B. Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol. 2008, 49:1711-1722.
21. Leshem Y. Nitric Oxide in Plants: Occurrence, Function and Use 2000, Kluwer Academic Publishers, Dordrecht, The Netherlands.
22. Mlíčková K., Luhová L., Lebeda A., Mieslerová B., Peč P. Reactive oxygen species generation and peroxidase activity during Oidium neolycopersici infection on Lycopersicon species. Plant Physiol. Biochem. 2004, 42:753-761.
23. Tománková K., Luhová L., Petřivalský M., Peč P., Lebeda A. Biochemical aspects of reactive oxygen species formation in the interaction between Lycopersicon spp. and Oidium neolycopersici. Physiol. Mol. Plant Pathol. 2006, 68:22-32.
24. Piterková J., Petřivalský M., Luhová L., Mieslerova B., Sedlářová M., Lebeda A. Local and systemic production of nitric oxide in tomato responses to powdery mildew infection. Mol. Plant Pathol. 2009, 10:501-513.
25. Mieslerová B., Lebeda A., Kennedy R. Variation in Oidium neolycopersici development on host and non-host plant species and their tissue defence responses. Ann. Appl. Biol. 2004, 144:237-248.
26. Wimmer B., Lottspeich F., van der Klei I., Veenhuis M., Gietl C. The glyoxysomal and plastid molecular chaperones (70-kDa heat shock protein) of watermelon cotyledons are encoded by a single gene. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:13624-13629.
27. Cheong Y.H., Chang H.-S., Gupta R., Wang X., Zhu T., Luan S. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 2002, 129:661-677.
28. Orozco-Cardenas M.L., Ryan C.A. Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiol. 2002, 130:487-493.
29. Byth H.-A., Kuun K.G., Bornman L. Virulence-dependent induction of Hsp70/Hsc70 in tomato by Ralstonia solanacearum. Plant Physiol. Biochem. 2001, 39:697-705.
30. Snyman M., Cronjé M.J. Modulation of heat shock factors accompanies salicylic acid-mediated potentiation of Hsp70 in tomato seedlings. J. Exp. Bot. 2008, 59:2125-2132.
31. Li Q.-B., Haskell D., Guy C. Coordinate and non-coordinate expression of the stress 70 family and other molecular chaperones at high and low temperature in spinach and tomato. Plant Mol. Biol. 1999, 39:21-34.
32. Garavaglia B., Garofalo C., Orellano E., Ottado J. Hsp70 and Hsp90 expression in citrus and pepper plants in response to Xanthomonas axonopodis pv. citri. Eur. J. Plant Pathol. 2009, 123:91-97.
33. Alamillo J., Almoguera C., Bartels D., Jordano J. Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum. Plant Mol. Biol. 1995, 29:1093-1099.
34. Mallouk Y., Vayssier-Taussat M., Bonventre J.V., Polla B.S. Heat shock protein 70 and ATP as partners in cell homeostasis. Int. J. Mol. Med. 1999, 4:463-474.
35. Bhattacharyya T., Karnezis A.N., Murphy S.P., Hoang T., Freeman B.C., Phillips B., Morimoto R.I. Cloning and subcellular localization of human mitochondrial hsp70. J. Biol. Chem. 1995, 270:1705-1710.
36. Felts S.J., Owen B.A.L., Nguyen P., Trepel J., Donner D.B., Toft D.O. The hsp90-related protein TRAP1 is a mitochondrial protein with distinct functional properties. J. Biol. Chem. 2000, 275:3305-3312.
37. Hua G., Zhang Q., Fan Z. Heat shock protein 75 (TRAP1) antagonizes reactive oxygen species generation and protects cells from granzyme M-mediated apoptosis. J. Biol. Chem. 2007, 282:20553-20560.
38. Kim Y.-M., de Vera M.E., Watkins S.C., Billiar T.R. Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-induced apoptosis by inducing heat shock protein 70 expression. J. Biol. Chem. 1997, 272:1402-1411.
39. Xu Q., Hu Y., Kleindienst R., Wick G. Nitric oxide induces heat-shock protein 70 expression in vascular smooth muscle cells via activation of heat shock factor 1. J. Clin. Invest. 1997, 100:1089-1097.
40. Manucha W., Vallés P. Hsp70/nitric oxide relationship in apoptotic modulation during obstructive nephropathy. Cell Stress Chaperones 2008, 13:413-420.
41. Yang J., Yun J.-Y., Zhang T.-H., Zhao H.L. Presoaking with nitric oxide donor SNP alleviates heat shock damages in mung bean leaf discs. Bot. Stud. 2006, 47:136.
42. Beligni M.V., Lamattina L. Nitric oxide protects against cellular damage produced by methylviologen herbicides in potato plants. Nitric Oxide 1999, 3:199-208.
43. Song L., Ding W., Shen J., Zhang Z., Bi Y., Zhang L. Nitric oxide mediates abscisic acid induced thermotolerance in the calluses from two ecotypes of reed under heat stress. Plant Sci. 2008, 175:826-832.
44. Prasad T.K., Anderson M.D., Martin B.A., Stewart C.R. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 1994, 6:65-74.
45. Foyer C.H., Lopez-Delgado H., Dat J.F., Scott I.M. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol. Plantarum 1997, 100:241-254.
46. 2: role of thioredoxin. Biochem. J. 1996, 318:187-193.
47. Mittler R., Zilinskas B.A. Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J. Biol. Chem. 1992, 267:21802-21807.
48. Davletova S., Rizhsky L., Liang H.J., Zhong S.Q., Oliver D.J., Coutu J., Shulaev V., Schlauch K., Mittler R. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 2005, 17:268-281.
49. Pnueli L., Liang H., Rozenberg M., Mittler R. Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J. 2003, 34:187-203.
50. Klessig D.F., Durner J., Noad R., Navarre D.A., Wendehenne D., Kumar D., Zhou J.M., Shah J., Zhang S., Kachroo P., Trifa Y., Pontier D., Lam E., Silva H. Nitric oxide and salicylic acid signaling in plant defense. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8849-8855.
51. Zottini M., Costa A., De Michele R., Ruzzene M., Carimi F., Lo Schiavo M. Salicylic acid activates nitric oxide synthesis in Arabidopsis. J. Exp. Bot. 2007, 58:1397-1405.
52. Cronjé M.J., Bornman L. Salicylic acid influences Hsp70/Hsc70 expression in Lycopersicon esculentum: dose- and time-dependent induction or potentiation. Biochem. Biophys. Res. Commun. 1999, 265:422-427.
53. Cronjé M.J., Weir I.E., Bornman L. Salicylic acid-mediated potentiation of Hsp70 induction correlates with reduced apoptosis in tobacco protoplasts. Cytometry 2004, 61:76-87.