Abstract
Kochia sieversiana (Pall.) C.A. Mey. is a forage plant that can grow in extremely alkalinized grasslands at pH 10 or higher. Accumulation of a large amount of oxalic acid (OxA) is a primary characteristic of K. sieversiana. In our study, seedlings of K. sieversiana were exposed to the following conditions: non-stress, salinity (200 mM, a molar ratio of NaCl and Na2SO4 1:1), and alkali stress (200 mM, a molar ratio of NaHCO3 and Na2CO3 1:1). Growth, water content, content of organic acids (including OxA), Na+, and K+, and activities of some OxA metabolism-related enzymes were determined. Results show that glycolate oxidase was the key enzyme for OxA synthesis; however, the carboxylation of phosphoenolpyruvate (PEP) by PEP carboxylase (PEPC) probably played a minor role in the OxA-synthetic pathway. The pathway of L-ascorbic acid catabolism was not the main source of OxA accumulation, and the activity of oxalate oxidase (OxO) involved in OxA decomposition was not a limiting factor for inner OxA accumulation. Taken together, accumulation of a large amount of OxA are not related to the degradation and secretion function of OxO but largely depend upon its synthetic function.
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Abbreviations
- GO:
-
glycolate oxidase
- ICL:
-
isocitrate lyase
- L-AA:
-
L-ascorbic acid
- OA:
-
organic acid
- OxA:
-
oxalic acid
- OxO:
-
oxalate oxidase
- PEPC:
-
phosphoenolpyruvate carboxylase
References
Berna, A., Bernier, F.: Regulation by biotic and abiotic stress of a wheat germin gene encoding oxalate oxidase, a H2O2-producing enzyme. — Plant mol. Biol. 39: 539–549, 1999.
Booker, F.L., Reid, C.D., Brunschön-Harti, S., Fiscus, E.L., Miller, J.E.: Photosynthesis and photorespiration in soybean [Glycine max (L.) Merr.] chronically exposed to elevated carbon dioxide and ozone. — J. exp. Bot. 48: 1843–1852, 1997.
Bouthour, D., Hajjaji-Nasraoui, A., Saafi, L., Gouia, H., Chaffei-Haouari, C.: Effects of NaCl on growth and activity of enzymes involved in carbon metabolism in leaves of tobacco (Nicotiana rustica). — Afr. J. Biotechnol. 63: 12619–12629, 2012.
Brock, M., Darley, D., Textor, S., Buckel, W.: 2-Methylisocitrate lyases from the bacterium Escherichia coli and the filamentous fungus Aspergillus nidulansS: characterization and comparison of both enzymes. - Eur. J. Biochem. 268: 3577–3586, 2001.
Bradford, M. M.: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. — Anal. Biochem. 72: 248–254, 1976.
Burrows, G.E., Tyrl, R.J.: Chenopodiaceae Vent. - In: Burrows, G.E., Tyrl, R.J. (ed.): Toxic Plants of North America. Pp. 338–364. John Wiley and Sons, New York 2012.
Cassol, D., Cambraia, J., Ribeiro, C., Oliveira, J.A., Cardoso, F.B.: Citric acid secretion induced by aluminium in two Stylosanthes species. — Biol. Plant. 60: 572–578, 2016.
Chakraborty, N., Ghosh, R., Ghosh, S., Narula, K., Tayal, R., Datta, A., Chakraborty, S.: Reduction of oxalate levels in tomato fruit and consequent metabolic remodeling following overexpression of a fungal oxalate decarboxylase. — Plant Physiol. 162: 364–378, 2013.
Chang, C.C., Beevers, H.: Biogenesis of oxalate in plant tissues. — Plant Physiol. 43: 1821–1828, 1968.
Chen, Z., Geng, H.C., Wang, S.S., Ding, M.L., Chen, X.J., Chen, J.Y.: [Formation, degeneration and functions of oxalate in plant.] - Mol. Plant Breed. 6: 105–110, 2007. [In Chin.]
Davey, M.W., Van, Montagu, M.V., Inzé, D., Sanmartin, M., Kanellis, A., Smirnoff, N., Benzie, I.J.J., Strain, J.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.
Davies, D.D., Asker, H.: Synthesis of oxalic acid by enzymes from lettuce leaves. — Plant Physiol. 72: 134–138, 1983.
Debolt, S., Melino, V., Ford, C.M.: Ascorbate as a biosynthetic precursor in plants. — Ann. Bot. 99: 3–8, 2007.
Franceschi, V.R., Horner, H.T.: Calcium oxalate crystals in plants. — Bot. Rev. 46: 361–427, 1980.
Franceschi, V.R., Nakata, P.A.: Calcium oxalate in plants: formation and function. — Annu. Rev. Plant Biol. 56: 41–71, 2005.
Guo, R., Shi, L.X., Yang, Y.F.: Germination, growth, osmotic adjustment and ionic balance of wheat in response to saline and alkaline stresses. -Soil Sci. Plant Nutr. 55: 667–679, 2009.
Hassan, M.J., Shafi, M., Zhang, G.P., Zhu, Z.J., Qaisar, M.: The growth and some physiological responses of rice to Cd toxicity as affected by nitrogen form. — Plant Growth Regul. 54: 125–132, 2008.
Hurkman, W.J., Tanaka, C.K.: Effect of salt stress on Germin gene expression in barley roots. — Plant Physiol. 110: 971–977, 1996.
Kazumi, S., Frank, A., Loewus, F.A.: Conversion of Dglucosone to oxalic acid and L- (+) -tartaric acid in detached leaves of pelargonium. — Phytochemistry 31: 3341–3344, 1992.
Kostman, T.A., Tarlyn, N.M., Loewus, F.A., Francecschi, V.R.: Biosynthesis of L-ascorbic acid and conversion of carbons 1 and 2 of L-ascorbic acid to oxalic acid occurs within individual calcium oxalate crystal idioblasts. — Plant Physiol. 125: 634–640, 2001.
Lane, B.G., Dunwell, J.M., Ray, J.A., Schmitt, M.R., Cuming, A.C.: Germin, a protein marker of early plant development, is an oxalate oxidase. — J. biol. Chem. 268: 12239–12242, 1993.
Libert, B., Franceschi, V.R.: Oxalate in crop plants. — J. Agr. Food Chem. 35: 926–938, 1987.
Lissner, J., Schierup, H., Comin, F.A., Astorga, V.: Effect of climate on the salt tolerance of two Phragmites australis populations. — I. Growth, inorganic solutes, nitrogen relations and osmoregulation. - Aquat. Bot. 64: 317–333, 1999.
Ma, J.F., Zheng, S.J., Matsumoto, H., Hiradate, S.: Detoxifying aluminum with buckwheat. — Nature 390: 569–570, 1997.
Ma, Y., Guo, L.Q., Wang, H.X., Bai, B., Shi, D.C.: Accumulation, distribution, and physiological contribution of oxalic acid and other solutes in an alkali-resistant forage plant, Kochia sieversiana, during adaptation to saline and alkaline conditions. — J. Plant Nutr. Soil Sci. 174: 655–663, 2011.
Ma, Z., Miyasaka, S.C.: Oxalate exudation by taro in response to Al. — Plant Physiol. 118: 861–865, 1998.
Mazen, A.M.A.: Calcium oxalate deposits in leaves of Corchorus olitorius as related to accumulation of toxic metals. — Russ. J. Plant Physiol. 51: 281–285, 2004.
Millerd, A., Morton, R.K., Wells, J.R.E.: Role of isocitrate lyase in synthesis of oxalic acid in plants. — Nature 196: 955–956, 1962.
Nakata, P.A.: Advances in our understanding of calcium oxalate crystal formation and function in plants. — Plant Sci. 164: 901–909, 2003.
Naliwajski, M.R., Sklodowska, M.: The oxidative stress and antioxidant systems in cucumber cells during acclimation to salinity. — J. Plant Physiol. 58: 47–54, 2014.
Raven, J.A.: H+ and Ca2+ in phloem and symplast: relation of relative immobility of the ions to the cytoplasmic nature of the transport paths. — New Phytol. 79: 465–480, 1977.
Reid, R.J., Smith, F.A.: The cytoplasmic pH state. - In: Rengel Z. (ed.): Handbook of Plant Growth - pH as the Master Variable. Pp. 49–71. Marcel Dekker, New York 2001.
Thakur, M., Goyal, L., Pundir, C.S.: Discrete analysis of plasma oxalate with alkylamine glass bound sorghum oxalate oxidase and horseradish peroxidase. — J. biochem. biophys. Methods 44: 77–88, 2000.
Tian, H., Jiang, L.R., Liu, E., Zhang, J.J., Liu, F., Peng, X.X.: Dependence of nitrate-induced oxalate accumulation on nitrate reduction in rice leaves. — Physiol. Plant. 133: 180–18, 2008.
Wang, G.Y., Yang, X.L., Tian, L.X.: Determination of total ascorbic acid in fruits, vegetables and derived products - flourometric method and colorimetric method. - In: Wang, G.Y., Yang, X.L., Tian, L.X. (ed.): National Standards of the People's Republic of China. Pp. 1–6. China Standards Press, Beijing 2004.
Xu, H.W., Ji, X.M., He, Z.H., Shi, W.P., Zhu, G.H., Niu, J.K., Li, B.S., Peng, X.X.: Oxalate accumulation and regulation is independent of glycolate oxidase in rice leaves. — J. exp. Bot. 57: 1899–1908, 2006.
Xu, L.H., Wang, W.Y., Guo, J.J., Qin, J., Shi, D.Q., Li, Y.L., Xu, J.: Zinc improves salt tolerance by increasing reactive oxygen species scavenging and reducing Na+ accumulation in wheat seedlings. — J. Plant Physiol. 58: 751–757, 2014.
Yang, C.W., Shi, D.C., Wang, D.L.: Comparative effects of salt stress and alkali stress on growth, osmotic adjustment and ionic balance of an alkali resistant halophyte Suaeda glauca (Bge.). — Plant Growth Regul. 56: 179–190, 2008.
Yang, Y.Y., Jung, J.Y., Song, W.Y., Suh, H.S., Lee, Y.S.: Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. — Plant Physiol. 124: 1019–1026, 2000.
Yang, Z.M., Yang, H., Wang, J., Wang, Y.S.: Aluminum regulation of citrate metabolism for Al-induced citrate efflux in the roots of Cassia tora L. - Plant Sci. 166:1589–1594, 2004.
Zhai, Y.J., Feng, X.H., Kang, Y.G.: [Pharmacognostical identification of fructus Kochia sieversiana.] - J. Chin. Med. Mater. 6: 283–285, 1996. [In Chin.]
Zhang, L., Wang, Z., Xia, Y., Guo, Y.K., Chen, W.S., Tang, K.X.: Metabolic engineering of plant L-ascorbic acid biosynthesis: recent trends and applications. — Crit. Rev. Biotechnol. 27: 173–182, 2007.
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Acknowledgements: We thank the International Science Editing (ISE) for language editing. This work was supported by the open fund from National Key Laboratory of Northeast Normal University (130028691).
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Ma, Y., Wang, X.P., Zhang, S.F. et al. Effects of salt and alkali stress on growth, accumulation of oxalic acid, and activity of oxalic acid-metabolizing enzymes in Kochia sieversiana . Biol Plant 60, 774–782 (2016). https://doi.org/10.1007/s10535-016-0650-2
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DOI: https://doi.org/10.1007/s10535-016-0650-2