biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 56:422-430, 2012 | DOI: 10.1007/s10535-012-0072-8

Involvement of G6PDH in heat stress tolerance in the calli from Przewalskia tangutica and Nicotiana tabacum

H. Gong1,2, G. Chen1,3, F. Li1, X. Wang1, Y. Hu1, Y. Bi1,3,*
1 School of Life Sciences, Lanzhou University, Lanzhou, P.R. China
2 School of Life Science and Technology, Lanzhou University of Technology, Lanzhou, P.R. China
3 Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, P.R. China

Glucose-6-phosphate dehydrogenase (G6PDH) has been implicated in supplying reduced nicotine amide cofactors for biochemical reactions and in modulating the redox state of cells. In this study, the role of G6PDH in thermotolerance of the calli from Przewalskia tangutica and tobacco (Nicotiana tabacum L.) was investigated. Results showed that Przewalskia tangutica callus was more sensitive to heat stress than tobacco callus. The activity of G6PDH and antioxidant enzymes (ascorbate peroxidase, catalase, peroxidase and superoxide dismutase) in calli from Przewalskia tangutica and tobacco increased after 40 °C treatment, although two calli exhibited a difference in the degree and timing of response to heat stress. When G6PDH was partially inhibited by glucosamine pretreatment, the antioxidant enzyme activities and thermotolerance in both calli significantly decreased. Simultaneously, the heat-induced H2O2 content and the plasma membrane NADPH oxidase activity were also reduced. Application of H2O2 increased the activity of G6PDH and antioxidant enzymes in both calli. Diphenylene iodonium, a NADPH oxidase inhibitor, counteracted heatinduced H2O2 accumulation and reduced the heat-induced activity of G6PDH and antioxidant enzymes. Moreover, exogenous H2O2 was effective in restoring the activity of G6PDH and antioxidant enzymes after glucosamine pretreatment. Western blot analysis showed that G6PDH gene expression in both calli was also stimulated by heat and H2O2, and blocked by DPI and glucosamine under heat stress. Taken together, under heat stress G6PDH promoted H2O2 accumulation via NADPH oxidase and the elevated H2O2 was involved in regulating the activity of antioxidant enzymes, which in turn facilitate to maintain the steady-state H2O2 level and protect plants from the oxidative damage.

Keywords: antioxidant enzymes; hydrogen peroxide; tobacco
Subjects: antioxidant enzymes; hydrogen peroxide; glucose-6-phosphate dehydrogenase; temperature - high; in vitro culture; callus; electrolyte leakage; ascorbate peroxidase; catalase; peroxidases; superoxide dismutase; NADPH oxidase; Western blot

Received: January 7, 2011; Accepted: June 26, 2011; Published: September 1, 2012  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Gong, H., Chen, G., Li, F., Wang, X., Hu, Y., & Bi, Y. (2012). Involvement of G6PDH in heat stress tolerance in the calli from Przewalskia tangutica and Nicotiana tabacum. Biologia plantarum, 56(3), 422-430. doi: 10.1007/s10535-012-0072-8
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Antonio, F.T., Ravindar, K., Royal, B.I., Arthur, W.G.: Correlation between polyamines and pyrrolidine alkaloids in developing tobacco callus. - Plant Physiol. 78: 323-326, 1985. Go to original source...
    2. Batz, O., Logemann, E., Reinold, S., Hahlbrock, K.: Extensive reprogramming of primary and secondary metabolism by fungal elicitor or infection in parsley cells. - Biol. Chem. 379: 1127-1135, 1998. Go to original source...
    3. Beauchamp, C., Fridovich, I.: Superoxide dismutase improved assays and an assay applicable to acrylamide gels. - Anal. Biochem. 44: 276-287, 1971. Go to original source...
    4. Bowsher, C.G., Hucklesby, D.P., Emes, M.J.: Nitrite reduction and carbohydrate metabolism in plastids purified from roots of Pisum sativum L. - Planta 177: 359-366, 1989. Go to original source...
    5. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
    6. Chaitanya, K.V., Sundar, D., Masilamani, S., Ramachandra Reddy, A.R.: Variation in heat stress-induced antioxidant enzyme activities among three mulberry cultivars. - Plant Growth Regul. 36: 175-180, 2002. Go to original source...
    7. Dat, J.F., Foyer, C.H., Scott, I.M.: Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. - Plant Physiol. 118: 1455-1461, 1998. Go to original source...
    8. Durner, J., Klessing, D.F.: Salicylic acid is a modulator of tobacco and mammalian catalases. - J. biol. Chem. 271: 28492-28502, 1996. Go to original source...
    9. Esposito, S., Carfagna, S., Massaro, G., Vona, V., Di Martino Rigano, V.: Glucose-6-phosphate dehydrogenase in barley roots: kinetic properties and localization of the isoforms. - Planta 212: 627-634, 2001. Go to original source...
    10. Esposito, S., Carillo, E., Carfagna, S.: Ammonium metabolism stimulation of glucose-6-P dehydrogenase and phosphoenolpyruvate carboxylase in young barley roots. - J. Plant Physiol. 153: 61-66, 1998. Go to original source...
    11. Esposito, S., Massaro, G., Vona, V., Di Martino Rigano, V., Carfagna, S.: Glutamate synthesis in barley roots: the role of the plastidic glucose-6-phosphate dehydrogenase. - Planta 216: 639-647, 2003. Go to original source...
    12. Foyer, C.H., Noctor, G.: Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. - Plant Cell 17: 1866-1875, 2005. Go to original source...
    13. Glaser, B.L., Brown, D.H.: Purification and properties of Dglucose 6-phosphate dehydrogenase. - J. biol. Chem. 216: 67-79, 1955. Go to original source...
    14. Grigorova, B., Vaseva, I., Demirevska, K., Feller, U.: Combined drought and heat stress in wheat: changes in some heat shock proteins. - Biol. Plant. 55: 105-111, 2011. Go to original source...
    15. Hammerschmidt, R., Nuckles, E.M., Kuc, J.: Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. - Physiol. Plant Pathol. 20: 73-82, 1982. Go to original source...
    16. Heckman, N.L., Horst, G.L., Gaussoin, R.E., Tavener B.T.: Trinexapac-ethyl influence on cell membrane thermostability of Kentucky bluegrass leaf tissue. - Sci. Hort. 92: 183-186, 2002. Go to original source...
    17. Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G., Mullineaux, P.: Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. - Science 284: 654-657, 1999. Go to original source...
    18. Kim, I.S., Moon, H.Y., Yun, H.S., Jin, I.: Heat shock causes oxidative stress and induces a variety of cell rescue proteins in Saccharomyces cerevisiae KNU5377. - J. Microbiol. 44: 492-501, 2006.
    19. Kletzien, R.F., Harris, P.K., Foellmi, L.A.: Glucose-6- phosphate dehydrogenase: a "housekeeping" enzyme subject to tissue-specific regulation by hormones, nutrients, and oxidant stress. - FASEB J. 8: 174-181, 1994. Go to original source...
    20. Königshofer, H., Tromballa, H.W., Löppert, H.G.: Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production. - Plant Cell Environ. 31: 1771-1780, 2008. Go to original source...
    21. Krüger, N.J., Von Schaewen, A.: The oxidative pentose phosphate pathway: structure and organization. - Curr. Opin. Plant Biol. 6: 236-246, 2003. Go to original source...
    22. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. - Nature 227: 680-685, 1970. Go to original source...
    23. Laloi, C., Apel, K., Danon, A.: Reactive oxygen signalling: the latest news. - Curr. Opin. Plant Biol. 7: 23-328, 2004. Go to original source...
    24. Liao, Y., Wei, Z.H., Bai, L., Deng, Z., Zhong, J.J.: Effect of fermentation temperature on validamycin A production by Streptomyces hygroscopicus 5008. - J. Biotechnol. 142: 271-274, 2009. Go to original source...
    25. Liu, Y.G., Wu, R.R., Wan, Q., Xie, G.Q., Bi, Y.R.: Glucose-6- phosphate dehydrogenase plays a pivotal role in nitric oxide-involved defense against oxidative stress under salt stress in red kidney bean roots. - Plant Cell Physiol. 48: 511-522, 2007. Go to original source...
    26. Locato, V., De Pinto, M.C., De Gara, L.: Different involvement of the mitochondrial, plastidial and cytosolic ascorbateglutathione redox enzymes in heat shock responses. - Physiol. Plant. 135: 296-306, 2009. Go to original source...
    27. Locato, V., Gadaleta, C., De Gara, L., De Pinto, M.C.: Production of reactive species and modulation of antioxidant network in response to heat shock: a critical balance for cell fate. - Plant Cell Environ. 31: 1606-1619, 2008. Go to original source...
    28. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M.A., Shulaev, V., Dangl, J.L., Mittler, R.: The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. - Sci. Signal. 2: 1-10, 2009. Go to original source...
    29. Mishra, Y., Bhargava, P., Chand Rai, L.C.: Differential induction of enzymes and antioxidants of the antioxidative defense system in Anabaena doliolum exposed to heat stress. - J. Therm. Biol. 30: 524-531, 2005. Go to original source...
    30. Mitra, R., Bhatia, C.R.: Bioenergetic cost of heat tolerance in wheat crop. - Curr. Sci. 94: 1049-1053, 2008.
    31. Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassay with tobacco tissue cultures. - Physiol. Plant 15: 473-497, 1962. Go to original source...
    32. Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 22: 867-880, 1981.
    33. Nemoto, Y., Sasakuma, T.: Specific expression of glucose-6- phosphate dehydrogenase (G6PDH) gene by salt stress in wheat (Triticum aestivum L.). - Plant Sci. 158: 53-60, 2000. Go to original source...
    34. Oji, Y., Watanabe, M., Wakiuchi, N., Okamoto, S.: Nitrite reduction in barley-root plastids: dependence on NADPH coupled with glucose-6-phoshate and 6-phosphogluconate dehydrogenases, and possible involvement of an electron carrier and a diaphorase. - Planta 165: 85-90, 1985. Go to original source...
    35. Pandolfi, P.P., Sonati, F., Rivi, R., Mason, P., Grosveld, F., Luzzatto, L.: Targeted disruption of the housekeeping gene encoding glucose 6-phosphate dehydrogenase (G6PD): G6PD is dispensable for pentose synthesis but essential for defense against oxidative stress. - EMBO J. 14: 5209-5215, 1995. Go to original source...
    36. 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 6: 65-74, 1994. Go to original source...
    37. Pugin, A., Frachisse, J.M., Tavernier, E., Bligny, R., Gout, E., Douce, R., Guern, J.: Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. - Plant Cell 9: 2077-2091, 1997. Go to original source...
    38. Qiu, Q.S., Su, X.F. The influence of extracellular-side Ca2+ on the activity of the plasma membrane H+-ATPase from wheat roots. - Aust. J. Plant Physiol. 25: 923-928, 1998. Go to original source...
    39. Rainwater, D.T., Gossett, D.R., Millhollon, E.P., Hanna, H.Y., Banks, S.W., Lucas, M.C.: The relationship between yield and the antioxidant defence system in tomatoes grown under heat stress. - Free Radical Res. 25: 421-435, 1996. Go to original source...
    40. Ren, X.N., Ma, Y.J., Zhou, M., Huo, S.H., Yao, J.L., Chen, H.: Determination of tropane alkaloid components in Przewalskia tangutica Maxim. by capillary electrophoresis with electrochemiluminescence detection. - Chin. J. Chromatogr. 26: 223-227, 2008. Go to original source...
    41. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S. Mittler, R.: When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. - Plant Physiol. 134: 1683-1696, 2004. Go to original source...
    42. Sagi, M., Fluhr, R.: Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. - Plant Physiol. 126: 1281-1290, 2001. Go to original source...
    43. Saidi, Y., Finka, A., Muriset, M., Bromberg, Z., Weiss, Y.G., Maathuis, F.J.M., Goloubinoff, P.: The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. - Plant Cell 21: 2829-2843, 2009. Go to original source...
    44. Sairam, R.K., Srivastava, G.C.: Changes in antioxidant activity in subcellular fraction of tolerant and susceptible wheat genotypes in response to long term salt stress. - Plant Sci. 162: 897-904, 2002. Go to original source...
    45. Sairam, R.K., Srivastava, G.C., Saxena, D.C.: Increased antioxidant activity under elevated temperature: a mechanism of heat stress tolerance in wheat genotypes. - Biol Plant. 43: 245-251, 2000. Go to original source...
    46. Scharte, J., Schön, H., Tjaden, Z., Weis, E., Von Schaewen, A.: Isoenzyme replacement of glucose-6-phosphate dehydrogenase in the cytosol improves stress tolerance in plants. - Proc. nat. Acad. Sci. USA 106: 8061-8066, 2009. Go to original source...
    47. Simon-Plas, F., Elmayan, T., Blein, J.P.: The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. - Plant J. 31: 137-147, 2002. Go to original source...
    48. ©indelář, L., ©indelářová, M.: Correlation of viral RNA biosynthesis with glucose-6-phosphate dehydrogenase activity and host resistance. - Planta 215: 862-869, 2002. Go to original source...
    49. Tian, W.N., Braunstein, L.D., Pang, J., Stuhlmeier, K.M., Xi, Q.C., Tian, X., Stanton, R.C.: Importance of glucose-6-phosphate dehydrogenase activity for cell growth. - J. biol Chem. 273: 10609-10617, 1998. Go to original source...
    50. Tiburcio, A.F., Kaur-Sawhney, R., Ingersoll, R.B., Galston, A.W.: Correlation between polyamines and pyrrolidine alkaloids in developing tobacco callus. - Plant Physiol. 78: 323-326, 1985. Go to original source...
    51. Torres, M.A., Dangl, J.L., Jones, J.D.G.: Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. - Proc. nat. Acad. Sci. USA 99: 517-522, 2002. Go to original source...
    52. 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 shockinduced programmed cell death in tobacco bright-yellow 2 cells. - Plant Physiol. 134: 1100-1112, 2004. Go to original source...
    53. Valderrama, R., Corpas, F.J., Carreras, A., Gómez-Rodríguez, M.V., Chaki, M., Pedrajas, J.R., Fernández-Ocaña, A., Del-Río, L.A., Barroso, J.B.: The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. - Plant Cell Environ. 29: 1449-1459, 2006. Go to original source...
    54. Veljovic-Jovanovic, S.D., Noctor, G., Foyer, C.H.: Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate. - Plant Physiol. Biochem. 40: 501-507, 2002. Go to original source...
    55. Volkov, R.A., Panchuk I.I., Mullineaux P.M., Schöffl F.: Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. - Plant mol. Biol. 61: 733-746, 2006. Go to original source...
    56. Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R.: Heat tolerance in plants: an overview. - Environ. exp. Bot. 61: 199-223, 2007. Go to original source...
    57. Wang, X.M., Ma, Y.Y., Huang, C.H., Li, J.S., Wan, Q., Bi, Y.R.: Glucose-6-phosphate dehydrogenase plays a central role in modulating reduced glutathione levels in reed callus under salt stress. - Planta 227: 611-623, 2008. Go to original source...
    58. Xu, W.H., Chen, G.C., Zhou, G.Y., Sun, J., Lu, X.F.: Rapid propagation in a Tibetan medicine plant - Przewalskia tangutica. - Chin. Traditional Herbs Drugs 40: 297-300, 2008.
    59. Yang, D.Z., Zhang, Z.Y., Lu, A.M., Sun, K., Liu, J.Q.: Floral organogenesis and development of two taxa in tribe Hyoscyameae (Solanaceae) - Przewalskia tangutica and Hyoscyamus niger. - Acta bot. sin. 44: 889-894, 2002.
    60. Yang, Y.L., Zhang, F., He, W.L., Wang, X.M., Zhang, L.X.: Iron-mediated inhibition of H+-ATPase in plasma membrane vesicles isolated from wheat roots. - Cell Mol. Life Sci. 60: 1249-1257, 2003. Go to original source...
    61. Zaka, R., Vandecasteele, C.M., Misset, M.T.: Effects of low chronic doses of ionizing radiation on antioxidant enzymes and G6PDH activities in Stipa capillata (Poaceae). - J. exp. Bot. 53: 1979-1987, 2002. Go to original source...

    Return to the content