Abstract
We even reported that hydrogen peroxide (H2O2) acts upstream of nitric oxide (NO) in the heat shock (HS) pathway in Arabidopsis (Arabidopsis thaliana) seedlings. In this work, we found a strange phenomenon that exogenous application of high concentration of H2O2 could not elevate internal H2O2 level under HS. NO donors sodium nitroprusside (SNP) and S-nitroso-N-acetylpenicillamine (SNAP) intensified this trend, whereas a special NO scavenger, 2-(4-phenyl)-4,4,5,5-tetramethyl-imidazoline-1-oxyl-3-oxyde (cPTIO) counteracted it, suggesting NO effects on reducing H2O2 accumulation. Western blotting and real-time reverse transcription-polymerase chain reaction demonstrated that NO eliminated H2O2 effects on the DNA-binding activity of HS factors and the accumulation of HS proteins. Subsequent experiments revealed that under HS, SNP and SNAP enhanced the activities of antioxidant enzymes catalase, ascorbate peroxidase and glutathione reductase, whereas c-PTIO inhibited them. Collectively, H2O2-induced NO stimulated the activities of antioxidant enzymes so as to eliminate excessive H2O2 in plant and then inhibit HS factor DNA-binding activity and HS protein accumulation, indicating a feedback inhibition between NO and H2O2 in thermotolerance.
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References
Aebi H (1984) Catalase. In: Packer L (ed) Methods in enzymology. Academic Press, Orlando, pp 121–126
Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11:545–555
Asai S, Ohta K, Yoshioka H (2008) MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20:1390–1406
Banti V, Mafessoni F, Loreti E, Alpi A, Perata P (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 152:1471–1483
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantity of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281
Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071
González A, Cabrera MDLA, Henríquez MJ, Contreras RA, Morales B, Moenne A (2012) Cross talk among calcium, hydrogen peroxide, and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases in Ulva compressa exposed to copper excess. Plant Physiol 158:1451–1462
Grace SC, Logan BA (1996) Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. Plant Physiol 112:1631–1640
Kolbert Z, Pető A, Lehotai N, Feigl G, Ördög A, Erdei L (2012) In vivo and in vitro studies on fluorophore specificity. Acta Biol Szeged 56:37–41
Kotak S, Larkindale J, Lee U, van Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316
Liu HT, Sun DY, Zhou RG (2005) Ca2+ and AtCaM3 are involved in the expression of heat shock protein gene in Arabidopsis. Plant Cell Environ 28:1276–1284
Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nover L, Bharti K, Döring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6:177–189
Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, Rodermel S, Inzé D, Mittler R (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32:329–342
Sang J, Jiang M, Lin F, Xu S, Zhang A, Tan M (2008) Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular anti-oxidant defense in maize plants. J Integr Plant Biol 50:231–243
Sebastiani M, Giordano C, Nediani C, Travaglini C, Borchi E, Zani M, Feccia M, Mancini M (2007) Induction of mitochondrial biogenesis is a maladaptive mechanism in mitochondrial cardiomyopathies. J Am Coll Cardiol 50:1362–1369
Sun J, Li L, Liu M, Wang M, Ding M, Deng S, Lu C, Zhou X, Shen X, Zheng X, Chen S (2010) Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tissue Organ Cult 103:205–215
Volkov RA, Panchuk II, Mullineaux PM, Schöffl F (2006) Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61:733–746
Wang XZ, Khaleque MA, Zhao MJ, Zhong R, Gaestel M, Calderwood SK (2006) Phosphorylation of HSF1 by MAPK-activated protein kinase 2 on serine 121 inhibits transcriptional activity and promotes HSP90 binding. J Biol Chem 281:782–791
Wang Y, Ries A, Wu K, Yang A, Crawford NM (2010) The Arabidopsis prohibitin gene PHB3 functions in nitric oxide—mediated responses and in hydrogen peroxide—induced nitric oxide accumulation. Plant Cell 22:249–259
Wang L, Guo Y, Jia L, Chu H, Zhou S, Chen K, Wu D, Zhao L (2014) Hydrogen peroxide acts upstream of nitric oxide in the heat shock pathway in Arabidopsis seedlings. Plant Physiol 164:2184–2196
Waters ER, Lee GJ, Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47:325–338
Xuan Y, Zhou S, Wang L, Cheng Y, Zhao L (2010) Nitric oxide functions as a signal and acts upstream of AtCaM3 in thermotolerance in Arabidopsis seedlings. Plant Physiol 153:1895–1906
Zhang H, Li YH, Hu LY, Wang SH, Zhang FQ, Hu KD (2008) Effects of exogenous nitric oxide donor on antioxidant metabolism in wheat leaves under aluminum stress. Russ J Plant Physiol 55:469–474
Zhang L, Zhou S, Xuan Y, Sun M, Zhao L (2009) Protective effect of nitric oxide against oxidative damage in Arabidopsis leaves under ultraviolet-B irradiation. J Plant Biol 52:135–140
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This work was supported by Opening Topic Fund Subsidization of State Key Laboratory of Crop Stress Biology in Arid Areas, China (Grant No. CSBAA2014003) and the Natural Science Foundation of China (Grant No. 31370301).
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Wu, D., Chu, H., Jia, L. et al. A feedback inhibition between nitric oxide and hydrogen peroxide in the heat shock pathway in Arabidopsis seedlings. Plant Growth Regul 75, 503–509 (2015). https://doi.org/10.1007/s10725-014-0014-x
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DOI: https://doi.org/10.1007/s10725-014-0014-x