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Magnesium deficiency-induced changes in organic acid metabolism of Citrus sinensis roots and leaves

  • Published:
Biologia Plantarum

Abstract

Organic acid (OA) metabolisms are of fundamental importance but very limited data are available on the responses of plant OA metabolisms to Mg-deficiency. Seedlings of Citrus sinensis (L.) Osbeck cv. Xuegan were irrigated with Mg-deficient (0, 50, or 500 μM MgSO4) or Mg-sufficient (2000 μM MgSO4) nutrient solution every other day for 12 weeks. Thereafter, we investigated the content of Mg, malate, and citrate as well as the activities of acidmetabolizing enzymes in roots and leaves. Root malate content remained stable except for an increase in the highest Mg content and root citrate content increased with increasing root Mg content. As leaf Mg content increased, leaf malate and malate + citrate content decreased whereas leaf citrate content increased. Mg-deficiency decreased or did not affect activities of citrate synthase (CS), aconitase (ACO), phosphoenolpyruvate carboxylase (PEPC), NADP-isocitrate dehydrogenase (NADP-IDH), NAD-malate dehydrogenase (NAD-MDH), NADP-malic enzyme (NADP-ME), and pyruvate kinase (PK) in roots, whereas phosphoenolpyruvate phosphatase (PEPP) activity slightly increased. In contrast, Mg-deficient leaves had higher or similar activities of enzymes above mentioned except PEPP, NAD-MDH, and NADP-ME. In conclusion, both glycolysis and tricarboxylic acid (TCA) cycle may be up-regulated in Mg-deficient leaves but down-regulated in Mg-deficient roots.

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Abbreviations

ACO:

aconitase

CS:

citrate synthase

NAD-MDH:

NAD-malate dehydrogenase

NADP-IDH:

NADP-isocitrate dehydrogenase

NADP-ME:

NADP-malic enzyme

OA:

organic acid

PEPC:

phosphoenolpyruvate carboxylase

PEPP:

phosphoenolpyruvate phosphatase

PK:

pyruvate kinase

References

  • Achituv, M., Bar-Akiva, A.: Metabolic pathway of α-ketoglutarate in citrus leaves as affected by phosphorus nutrition. - Plant Physiol. 61: 703–705, 1978.

    Article  PubMed  CAS  Google Scholar 

  • Besford, R.T.: Use of pyruvate kinase activity of leaf extracts for the quantitative assessment of potassium and magnesium status of tomato plants. - Ann. Bot. 42: 317–324, 1978.

    CAS  Google Scholar 

  • Bottrill, D.E., Possingham, J.V., Kriedemann, P.E.: The effect of nutrient deficiencies on photosynthesis and respiration in spinach. - Plant Soil 32: 428–438, 1970.

    Article  Google Scholar 

  • Büchert, A.M., Civello, P.M., Martínez, G.A.: Characterization of Mg-dechelating substance in senescent and pre-senescent Arabidopsis thaliana leaves. - Biol. Plant. 55: 75–82, 2011.

    Article  Google Scholar 

  • Cakmak, I., Kirkby, E.A.: Role of magnesium in carbon partitioning and alleviating photooxidative damage. - Physiol. Plant. 133: 692–704, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Cakmak, I., Hengeler, C., Marschner, H.: Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. - J. exp. Bot. 45: 1245–1250, 1994a.

    Article  CAS  Google Scholar 

  • Cakmak, I., Hengeler, C., Marschner, H.: Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. - J. exp. Bot. 45: 1251–1257, 1994b.

    Article  CAS  Google Scholar 

  • Chen, L.S., Lin, Q., Nose, A.: A comparative study on diurnal changes in metabolite levels in the leaves of three crassulacean acid metabolism (CAM) species, Ananas comosus, Kalanchoë daigremontiana and K. pinnata. - J. exp. Bot. 53: 341–350, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Epstein, E., Bloom, A.J. (ed.): Mineral Nutrition of Plants: Principles and Perspectives. 2nd Ed. - Sinauer Associates, Sunderland 2004.

    Google Scholar 

  • Emmerlich, V., Linka, N., Reinhold, T., Hurth, M.A., Traub, M., Martinoia, E., Neuhaus, H.E.: The plant homolog to the human sodium/dicarboxylic cotransporter is the vacuolar malate carrier. - Proc. nat. Acad. Sci. USA 100: 11122–11126, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Fischer, E.S.: Photosynthetic irradiance response curves of Phaseolus vulgaris under moderate or severe magnesium deficiency. - Photosynthetica 33: 385–390, 1997.

    CAS  Google Scholar 

  • Fischer, E.S., Bremer, E.: Influence of magnesium deficiency on rates of leaf expansion, starch and sucrose accumulation, and net assimilation in Phaseolus vulgaris. - Physiol. Plant. 89: 271–276, 1993.

    Article  CAS  Google Scholar 

  • Fischer, E.S., Lohaus, G., Heineke, D., Heldt, H.W.: Magnesium deficiency results in accumulation of carbohydrates and amino acids in source and sink leaves of spinach. - Physiol. Plant. 102: 16–20, 1998.

    Article  CAS  Google Scholar 

  • Guha, S., Rao, I.S.: Nitric oxide promoted rhizome induction in Cymbidium shoot buds under magnesium deficiency. - Biol. Plant. 56: 227–236, 2012.

    Article  CAS  Google Scholar 

  • Hariadi, Y., Shabala, S.: Screening broad beans (Vicia faba) for magnesium deficiency. II. Photosynthetic performance and leaf bioelectrical responses. - Funct. Plant Biol. 31: 539–549, 2004.

    Article  CAS  Google Scholar 

  • Hermans, C., Bourgis, F., Faucher, M., Strasser, R.J., Delrot, S., Verbruggen, N.: Magnesium deficiency in sugar beets alters sugar partitioning and phloem loading in young mature leaves. - Planta 220: 541–549, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Hermans, C., Johnson, G.N., Strasser, R.J., Verbruggen, N.: Physiological characterisation of magnesium deficiency in sugar beet: acclimation to low magnesium differentially affects photosystems I and II. - Planta 220: 344–355, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Hermans, C., Verbruggen, N.: Physiological characterization of Mg deficiency in Arabidopsis thaliana. - J. exp. Bot. 56: 2153–2161, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Hoffland, E., Van den Boogaard, R., Nelemans, J., Findenegg, G.: Biosynthesis and root exudation of citric and malic acids in phosphate-starved rape plants. - New Phytol. 122: 675–680, 1992.

    Article  CAS  Google Scholar 

  • Hurth, M.A., Suh, S.J., Kretzschmar, T., Geis, T., Bregante, M., Gambale, F., Martinoia, E., Neuhaus, H.E.: Impaired pH homeostasis in Arabidopsis lacking the vacuolar dicarboxylate transporter and analysis of carboxylic acid transport across the tonoplast. - Plant Physiol. 137: 901–910, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Laing, W., Greer, D., Sun, O., Beets, P., Lowe, A., Payn, T.: Physiological impacts of Mg deficiency in Pinus radiata: growth and photosynthesis. - New Phytol. 146: 47–57, 2000.

    Article  CAS  Google Scholar 

  • Li, L., Tutone, A.F., Drummond, R.S.M., Gardner, R.C., Luan. S.: A novel family of magnesium transport genes in Arabidopsis. - Plant Cell 13: 2761–2775, 2001a.

    PubMed  CAS  Google Scholar 

  • Li, Y., Liu, X.H., Zhuang, W.M.: The effect of magnesium deficiency on photosynthesis of longan (Dimocarpus longan Lour.) seedlings. - Acta hort. sin. 28: 101–106, 2001b.

    Google Scholar 

  • Lin, Z.H., Chen, L.S., Chen, R.B., Zhang, F.Z., Jiang, H.X., Tang, N., Smith, B.R.: Root release and metabolism of organic acids in tea plants in response to phosphorus supply. - J. Plant Physiol. 168: 644–652, 2011.

    Article  PubMed  CAS  Google Scholar 

  • Ling, L.L., Peng, L.Z., Cao, L., Jiang, C.L., Chun, C.P., Zhang, G.Y., Wang, Z.X.: Effect of magnesium deficiency on photosynthesis characteristic of Beibei 447 Jinchen orange. - J. Fruit Sci. 26: 275–280, 2009.

    CAS  Google Scholar 

  • López-Bucio, J., Nieto-Jacobo, M.F., Ramírez-Rodríguez, V., Herrera-Estrella, L.: Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. - Plant Sci. 160: 1–13, 2000.

    Article  PubMed  Google Scholar 

  • Marschner, H. (ed.): Mineral Nutrition of Higher Plants. 2nd Ed. - Academic Press, San Diego 1995.

    Google Scholar 

  • Moing, A., Rothan, C., Svanella, L., Just, D., Diakou, P., Raymond, P., Gaudillere, J.-P., Monet, R.: Role of phosphoenolpyruvate carboxylase in organic acid accumulation during peach fruit development. - Physiol. Plant. 108: 1–10, 2000.

    Article  CAS  Google Scholar 

  • Peaslee, D.E., Moss, D.N.: Photosynthesis in K- and Mg-deficient maize (Zea mays L.) leaves. - Soil Sci. Soc. Amer. J. 30: 220–223, 1966.

    Article  CAS  Google Scholar 

  • Rentsch, D., Martinola, E.: Citrate transport into barley mesophyll vacuoles-comparison with malate-uptake activity. - Planta 184: 532–537, 1991.

    Article  CAS  Google Scholar 

  • Sadka, A., Dahan, E., Cohen, L., Marsh, K.B.: Aconitase activity and expression during the development of lemon fruit. - Physiol. Plant. 108: 255–262, 2000.

    Article  CAS  Google Scholar 

  • Salisbury, F.B., Ross, C.W.: Plant Physiology. 4th Ed. - Wadsworth Publishing Company, Belmont 1992.

    Google Scholar 

  • Schell, J.: Interdependence of pH, malate concentration, and calcium and magnesium concentrations in the xylem sap of beech roots. - Tree Physiol. 17: 479–483, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Shaul, O.: Magnesium transport and function in plants: the tip of the iceberg. - BioMetals 15: 309–323, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Tang, Q.Y., Feng, M.G. (ed.): DPS Data Processing System for Practical Statistics. 2nd Ed. - Chinese Science Press, Beijing 2002.

    Google Scholar 

  • Terry, N., Ulrich, A.: Effects of magnesium deficiency on the photosynthesis and respiration of leaves of sugar beet. - Plant Physiol. 54: 379–381, 1974.

    Article  PubMed  CAS  Google Scholar 

  • Wang, H., Ma, F., Cheng, L.: Metabolism of organic acids, nitrogen and amino acids in chlorotic leaves of ‘Honeycrisp’ apple (Malus domestica Borkh) with excessive accumulation of carbohydrates. - Planta 232: 511–522, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Yamaki, Y.T.: Organic acids in the juice of citrus fruits. - J. jap. Soc. hort. Sci. 58: 587–594, 1989.

    Article  CAS  Google Scholar 

  • Yang, G.D., Zhu, Z.J., Ji, Y.M.: Effect of light intensity and magnesium deficiency on chlorophyll fluorescence and active oxygen in cucumber leaves. - Plant Nutr. Fertil. Sci. 8: 115–118, 2002.

    Google Scholar 

  • Yang, G.H., Yang, L.T., Jiang, H.X., Wang, P., Chen, L.S.: Physiological impacts of magnesium-deficiency in Citrus seedlings: photosynthesis, antioxidant system and carbohydrates. - Trees Struct. Funct. 26: 1237–1250, 2012.

    Article  CAS  Google Scholar 

  • Yang, L.T., Jiang, H.X., Tang, N., Chen, L.S.: Mechanisms of aluminum-tolerance in two species of citrus: Secretion of organic acid anions and immobilization of aluminum by phosphorus in roots. - Plant Sci. 180: 521–530, 2011.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. College of Resources and Environmental Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    L.T. Yang, Y.B. Lu & L.S. Chen

  2. Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    L.T. Yang, G.H. Yang, X. You, C.P. Zhou, Y.B. Lu & L.S. Chen

  3. College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    L.T. Yang, C.P. Zhou & L.S. Chen

  4. College of Life Science, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    G.H. Yang & X. You

  5. Fujian Key Laboratory for Plant Molecular and Cell Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    L.S. Chen

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  1. L.T. Yang
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  2. G.H. Yang
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  3. X. You
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Correspondence to L.S. Chen.

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Acknowledgement

This work was supported by grants from the earmarked fund for China Agriculture Research System

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Yang, L., Yang, G., You, X. et al. Magnesium deficiency-induced changes in organic acid metabolism of Citrus sinensis roots and leaves. Biol Plant 57, 481–486 (2013). https://doi.org/10.1007/s10535-013-0313-5

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  • DOI: https://doi.org/10.1007/s10535-013-0313-5

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