biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 60:677-685, 2016 | DOI: 10.1007/s10535-016-0628-0

Suppression of tomato SlGGP aggravates methyl viologen-mediated oxidative stress

D.-Y. Yang1, N.-N. Ma1, Z.-M. Liu1, X.-C. Ma1, S.-J. Zhao1,*, Q.-W. Meng1,*
1 College of Life Science, State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai'an, Shandong, P.R. China

Ascorbate (AsA) is an important antioxidant that can scavenge reactive oxygen species to protect plant cells against oxidative stress. Guanosine 5'-diphosphate (GDP)-L-galactose phosphorylase (GGP) is a key enzyme in the AsA biosynthetic pathway. To investigate the functions of GGP in AsA synthesis and oxidative stress tolerance in tomato, antisense lines with a reduced expression of SlGGP were obtained. Photobleaching after treatment of leaf disks with methyl viologen was more severe in transgenic lines compared to wild type (WT) plants. Moreover, compared with the WT plants, the transgenic plants showed a higher content of hydrogen peroxide, superoxide anion, malondialdehyde, as well as ion leakage, but a lower content of AsA and chlorophylls, ascorbate peroxidase activity, net photosynthetic rate, and maximal photochemical efficiency of photosystem II. Results of real-time quantitative polymerase chain reaction show that suppression of the SlGGP gene in the transgenic plants reduced their oxidative stress tolerance.

Keywords: ascorbate; ascorbate peroxidase; chlorophyll; GDP-L-galactose phosphorylase; malondialdehyde; net photosynthetic rate; photosystem II; Solanum lycopersicum
Subjects: oxidative stress; methyl viologen; malondialdehyde; electrolyte leakage; net photosynthetic rate; chlorophyll content; chlorophyll fluorescence; ascorbate peroxidase; catalase; superoxide dismutase; tomato

Received: July 23, 2015; Revised: December 23, 2015; Accepted: January 22, 2016; Published: December 1, 2016  Show citation

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Yang, D.-Y., Ma, N.-N., Liu, Z.-M., Ma, X.-C., Zhao, S.-J., & Meng, Q.-W. (2016). Suppression of tomato SlGGP aggravates methyl viologen-mediated oxidative stress. Biologia plantarum60(4), 677-685. doi: 10.1007/s10535-016-0628-0
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References

  1. Agius, F., Gonzalez-Lamothe, R., Caballero, J.L., Munoz-Blanco, J., Botella, M.A., Valpuesta, V.: Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. - Nat. Biotechnol. 21: 177-181, 2003. Go to original source...
  2. Bulley, S.M., Rassam, M., Hoser, D., Otto, W., Schüneman, N., Wright, M., MacRae, E., Gleave, A., Laing, W.: Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP L-galactose guanyltransferase is a major control point of vitamin C biosynthesis. - J. exp. Bot. 60: 765-778, 2009. Go to original source...
  3. Conklin, P., Williams, E., Last, R.: Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. - Proc. natl. Acad. Sci. USA 93: 9970-9974, 1996. Go to original source...
  4. Cornic, G., Bukhov, N.G., Wiese, C., Bligny, R., Heber, U.: Flexible coupling between light-dependent electron and vectorial proton transport in illuminated leaves of C3 plants; role of photosystem I dependent proton pumping. - Planta 210: 468-477, 2000. Go to original source...
  5. Davey, M., Montagu, M., Inze, D., Sanmartin, M., Kanellis, A., Smirnoff, N., Benzie, I., Strain, J., Favell, D., Fletcher, J.: Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. - J. Sci. Food Agr. 80: 825-860, 2000. Go to original source...
  6. Gechev, T.S., Van, Breusegem, F., Stone, J.M., Denev, I., Laloi, C.: Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. - Bioassays 28: 1091-1101, 2006. Go to original source...
  7. Gilbert, L., Alhagdow, M., Nunes-Nesi, A., Quemener, B., Guillon, F., Bouchet, B., Faurobert, M., Gouble, B., Page, D., Garcia, V.: The GDP-D-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and noncellulosic cell wall biosynthesis in tomato. - Plant J. 60: 499-508, 2009. Go to original source...
  8. Hancock, R.D., Viola, R.: Biosynthesis and catabolism of Lascorbic acid in plants. - Crit. Rev. Plant Sci. 24: 167-188, 2005. Go to original source...
  9. Holuigue, L., Salinas, P., Blanco, F., Garreton, V.: Salicylic acid and reactive oxygen species in the activation of stress defense genes. - In: Hayat, S., Ahmad, A. (ed.): Salicylic Acid - a Plant Hormone. Pp. 197-246. Springer, Dordrecht 2007. Go to original source...
  10. Huang, C.H., He, W.L., Guo, J.K., Chang, X.X., Su, P.X., Zhang, L.X.: Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. - J. exp. Bot. 56: 3041-3049, 2005. Go to original source...
  11. Ishikawa, T., Shigeoka, S.: Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. - Biosci. Biotechnol. Biochem. 72: 1143-1154, 2008. Go to original source...
  12. Kwon, S.Y., Jeong, Y.J., Lee, H.S., Kim, J.S., Cho, K.Y., Allen, R.D., Kwark, S.S.: Enhanced tolerance of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. - Plant Cell Environ. 25: 873-882, 2002. Go to original source...
  13. Laing, W.A., Wright, M.A., Cooney, J., Bulley, S.M.: The missing step of the L-galactose pathway of ascorbate biosynthesis in plants, an L -galactose guanyltransferase, increases leaf ascorbate content. - Proc. nat. Acad. Sci. USA 104: 9534-9539, 2007. Go to original source...
  14. Li, F., Wu, Q.Y., Sun, Y.L., Wang, L.Y., Yang, X.H., Meng, Q.W.: Overexpression of chloroplastic monodehydroascorbate reductase enhanced tolerance to temperature and methylviologen-mediated oxidative stresses. - Physiol. Plant. 139: 421-434, 2010. Go to original source...
  15. Li, X.G.., Meng, Q.W., Jiang, G..Q., Zou, Q.: The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water-water cycle. - Photosynthetica 41: 259-265, 2003. Go to original source...
  16. Linster, C.L., Gomez, T.A., Christensen, K.C., Adler, L.N., Young, B.D., Brenner, C., Clarke, S.G.: Arabidopsis VTC2 encodes a GDP-L-galactose phosphorylase, the last unknown enzyme in the Smirnoff-Wheeler pathway to ascorbic acid in plants. - J. biol. Chem. 282: 18879-18885, 2007. Go to original source...
  17. Loewus, M.W., Bedgar, D.L., Saito, K., Loewus, F.L.: Conversion of L-sorbonone to L-ascorbic acid by a NADPdependent dehydrogenase in bean and spinach leaf. - Plant Physiol. 94: 1492-1495, 1990. Go to original source...
  18. Lorence, A., Chevone, B.I., Mendes, P., Nessler, C.L.: Myoinositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. - Plant Physiol. 134: 1200-1205, 2004. Go to original source...
  19. Mellidou, I., Chagne, D., Laing, W.A., Keulemans, J., Davey, M.W.: Allelic variation in paralogs of GDP-L-galactose phosphorylase is a major determinant of vitamin C concentrations in apple fruit. - Plant Physiol. 160: 1613-1629, 2012. Go to original source...
  20. Miller, G., Suzuki, N., Rizhsky, L., Hegie, A., Koussevitzky, S., Mittler, R.: Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. - Plant Physiol. 144: 1777-1785, 2007. Go to original source...
  21. Munné-Bosch, S., Alegre, L.: Interplay between ascorbic acid and lipophilic antioxidant defences in chloroplasts of waterstressed Arabidopsis plants. - FEBS Lett. 524: 145-148, 2002. Go to original source...
  22. Murik, O., Elboher, A., Kaplan, A.: Dehydroascorbate: a possible surveillance molecule of oxidative stress and programmed cell death in the green alga Chlamydomonas reinhardtii. - New Phytol. 202: 471-484, 2014. Go to original source...
  23. Noctor, G.: Metabolic signalling in defence and stress: the central roles of soluble redox couples. - Plant Cell Environ. 29: 409-425, 2006. Go to original source...
  24. Sasaki-Sekimoto, Y., Taki, N., Obayashi, T., Aono, M., Matsumoto, F., Sakurai, N., Ohta, H.: Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. - Plant J. 44: 653-668, 2005. Go to original source...
  25. Smirnoff, N., Conklin, P.L., Loewus, F.A.: Biosynthesis of ascorbic acid in plants: a renaissance. - Annu. Rev. Plant Physiol. Plant mol. Biol. 52: 437-467, 2001. Go to original source...
  26. Smirnoff, N.: Ascorbate biosynthesis and function in photoprotection. - Phil.. Trans. roy. Soc. London B. Biol. Sci. 355: 1455-1464, 2000. Go to original source...
  27. Van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. - Photosynth. Res. 25: 147-150, 1990. Go to original source...
  28. Wang, L.Y., Li, D., Deng, Y.S., Lv, W., Meng, Q.W.: Antisense-mediated depletion of tomato GDP-L-galactose phosphorylase increases susceptibility to chilling stress. - J. Plant Physiol. 170: 303-314, 2013. Go to original source...
  29. Wheeler, G., Jones, M., Smirnoff, N.: The biosynthetic pathway of vitamin C in higher plants. - Nature 393: 365-369, 1998. Go to original source...
  30. Wolucka, B.A., Goossens, A., Inze, D.: Methyl jasmonate stimulates the de novo biosynthesis of vitamin C in plant cell suspensions. - J. exp. Bot. 56: 2527-2538, 2005. Go to original source...
  31. Yoshimura, K., Miyao, K., Gaber, A., Takeda, T., Kanaboshi, H., Miyasaka, H., Shigeoka, S.: Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. - Plant J. 37: 21-33, 2004. Go to original source...
  32. Zhang, C., Ouyang, B., Yang, C., Zhang, X., Liu, H., Zhang, Y., Zhang, J., Li, H., Ye, Z.: Reducing AsA leads to leaf lesion and defence response in knock-down of the AsA biosynthetic enzyme GDP-D-mannose pyrophosphorylase gene in tomato plant. - PLoS ONE 8: e61987, 2013. Go to original source...
  33. Zhang, C.J., Liu, J.X., Zhang, Y.Y., Cai, X.F., Gong, P.J., Zhang, J.H., Wang, T.T., Li, H.X., Ye, Z.B.: Over-expression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. - Plant Cell Rep. 30: 389-398, 2010. Go to original source...
  34. Zhang, W., Gruszewski, H.A., Chevone, B.I., Nessler, C.L.: An Arabidopsis purple acid phosphatase with phytase activity increases foliar ascorbate. - Plant Physiol. 146: 431-440, 2008. Go to original source...