Abstract
Magnesium nutrition is often forgotten, while its absence adversely affects numerous functions in plants. Magnesium deficiency is a growing concern for crop production frequently observed in lateritic and leached acid soils. Competition with other cations (Ca2+, Na+, and K+) is also found to be an essential factor, inducing magnesium deficiency in plants. This nutrient is required for chlorophyll formation and plays a key role in photosynthetic activity. Moreover, it is involved in carbohydrate transport from source-to-sink organs. Hence, sugar accumulation in leaves that results from the impairment of their transport in phloem is considered as an early response to Mg deficiency. The most visible effect is often recorded in root growth, resulting in a significant reduction of root/shoot ratio. Carbohydrate accumulation in source leaves is attributed to the unique chemical proprieties of magnesium. As magnesium is a nutrient with high mobility in plants, it is preferentially transported to source leaves to prevent severe declines in photosynthetic activity. In addition, Mg is involved in the source-to-sink transport of carbohydrates. Hence, an inverse relationship between Mg shortage and sugar accumulation in leaves is often observed. We hereby review all these aspects with a special emphasis on the role of Mg in photosynthesis and the structural and functional effects of its deficiency on the photosynthetic apparatus.
Similar content being viewed by others
References
Aitken RL, Dickson T, Hailes KJ, Moody PW (1999) Response of field-grown maize to applied magnesium in acidic soil in northeastern Australia. Aust J Agric Res 50:191–198
Alexander EB, Coleman RG, Keeler-Wolf T, Harrison S (2007) Serpentine geoecology of Western North America: geology, soils, and vegetation. Oxford University Press, New York
Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59:1555–1568
Ayala-Silva T, Beyl CA (2005) Changes in spectral reflectance of wheat leaves in response to specific macronutrient deficiency. Adv Space Res 2:305–317
Balakrishnan K, Rajendran C, Kulandaivelu G (2001) Differential responses of iron, magnesium, and zinc deficiency on pigment composition, nutrient content, and photosynthetic activity in tropical fruit crops. Photosynthetica 38:477–479
Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60:43–73
Bedi AS, Sekhon GS (1977) Effect of potassium and magnesium application to soils on the dry-matter yield and cation composition of maize. J Agric Sci 88:735–758
Bergmann W (1992) Nutritional disorders of plants-Development, visual and analytical diagnosis. Gustav Fischer Verlag, Germany
Bowler C, Montagu MV, Inz D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116
Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266
Britto DT, Kronzucker HJ (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133:637–650
Broadley MR, White PJ (2010) Eats roots and leaves. Can edible horticultural crops address dietary calcium, magnesium and potassium deficiencies? Proc Nutr Soc 69:601–612
Broadley MR, Hammond JP, King GJ, Astley D, Bowen HC, Meacham MC et al (2008) Shoot calcium and magnesium concentrations differ between subtaxa, are highly heritable, and associate with potentially pleiotropic loci in Brassica oleracea. Plant Physiol 146:1707–1720
Bush DR (1989) Proton-coupled sucrose transport in plasmalemma vesicles isolated from sugar beet (Beta vulgaris L. cv. Great Western) leaves. Plant Physiol 89:1318–1323
Cakmak I, Kirkby EA (2008) Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 133:692–704
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227
Cakmak I, Yazici AM (2010) Magnesium: a forgotten element in crop production. Better Crops 94:23–25
Cakmak I, Hengeler C, Marschner H (1994a) 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
Cakmak I, Hengeler C, Marschner H (1994b) 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
Candan N, Tarhan L (2003) Relationship among chlorophyll-carotenoid content, antioxidant enzyme activities and lipid peroxidation levels by Mg2+ deficiency in the Mentha pulegium leaves. Plant Physiol Biochem 41:35–40
Ceppi MG, Oukarroum A, Nuran C, Strasser RJ, Schansker G (2012) The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plant 144:277–288
Cowan JA (2002) Structural and catalytic chemistry of magnesium dependent enzymes. Biometals 15:225–235
Dannehl H, Wietoska H, Heckmann H, Godde D (1996) Changes in D1-protein turnover and recovery of photosystem II activity precede accumulation of chlorophyll in plants after release from mineral stress. Planta 199:34–42
Deng W, Luo K, Li D, Zheng X, Wei X, Smith W, Thammina C, Lu L, Li Y, Pei Y (2006) Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance. J Exp Bot 57:4235–4243
Ding Y, Xu G (2011) Low magnesium with high potassium supply changes sugar partitioning and root growth pattern prior to visible magnesium deficiency in leaves of Rice (Oryza sativa L.). Am J Plant Sci 2:601–608
Ding Y, Luo W, Xu G (2006) Characterisation of magnesium nutrition and interaction of magnesium and potassium in rice. Ann Appl Biol 149:111–123
Ding Y, Chang C, Luo W, Wu Y, Ren X, Wang P, Xu G (2008) High potassium aggravates the oxidative stress induced by magnesium deficiency in rice leaves. Pedosphere 18:316–327
Ericsson T, Kahr M (1995) Growth and nutrition of birch seedlings at varied relative addition rates of magnesium. Tree Physiol 15:85–93
Farhat N, Rabhi M, Falleh H, Lengliz K, Smaoui A, Abdelly C, Lachaal M, Karray-Bouraoui N (2013) Interactive effects of excessive potassium and Mg deficiency on safflower. Acta Physiol Plant 35:2737–2745
Farhat N, Rabhi M, Krol M, Barhoumi Z, Ivanov AG, McCarthy A, Abdelly C, Smaoui A, Huner NPA (2014) Starch and sugar accumulation in Sulla carnosa leaves upon Mg2+ starvation. Acta Physiol Plant. doi:10.1007/s11738-014-1592-y
Farhat N, Ivanov AG, Krol M, Rabhi M, Smaoui A, Abdelly C, Hüner NPA (2015a) Preferential damaging effects of limited magnesium bioavailability on photosystem I in Sulla carnosa plants. Planta. doi:10.1007/s00425-015-2248-x
Farhat N, Sassi H, Zorrig W, Abdelly C, Barhoumi Z, Smaoui A, Rabhi M (2015b) Is excessive Ca the main factor responsible for Mg deficiency in Sulla carnosa on calcareous soils? J Soil Sediment. doi:10.1007/s11368-015-1101-y
Fink S (1993) Microscopic criteria for the diagnosis of abiotic injuries to conifer needles. In: Huettl RF, Mueller-Dombois D (eds) Forest decline in the Atlantic and Pacific region. Springer, Berlin, pp 175–189
Fischer ES (1997) Photosynthetic irradiance curves of Phaseolus vulgaris under moderate or severe magnesium deficiency. Photosynthetica 33:385–390
Fischer ES, Bremer E (1993) Influence of magnesium deficiency on rates of leaf expansion, starch and sucrose accumulation and net assimilation in Phaseolus vulgaris. Physiol Plantarum 89:271–276
Fischer ES, Lohaus G, Heineke D, Heldt HW (1998) Magnesium deficiency resulted in accumulation of carbohydrates and amino acids in source and sink leaves of spinach. Physiol Plantarum 102:16–20
Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signalling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875
Gao C, Zhao Q, Jianga L (2015) Vacuoles protect plants from high magnesium stress. PNAS 112:2931–2932
Gardner RC (2003) Genes for magnesium transport. Curr Opin Plant Biol 6:263–267
Godde D, Dannehl H (1994) Stress-induced chlorosis and increase in D1-protein turnover precede photoinhibition in spinach suffering under magnesium/sulphur deficiency. Planta 195:291–300
Gransee A, Führs H (2013) Magnesium mobility in soils as a challenge for soil and plant analysis, magnesium fertilization and root uptake under adverse growth conditions. Plant Soil 368:5–21
Grusak MA, Deltrot S, Ntsika G (1990) Short-term effect of heat-girdles on source leaves of Vicia faba. J Exp Bot 41:1371–1377
Grzebisz W (2011) Magnesium-food and human health. J Elem 16:299–323
Guo W, Chen S, Hussain N, Cong Y, Liang Z, Chen K (2015) Magnesium stress signaling in plant: just a beginning. Plant Signal Behav. doi:10.4161/15592324.2014.992287
Hailes KJ, Aitken RL, Menzies NW (1997) Magnesium in tropical and subtropical soils from north-eastern Australia. II. Response by glasshouse-grown maize to applied magnesium. Aust J Soil Res 35:629–641
Hannick AF, Waterkeyn L, Weissen F, van Prag HJ (1993) Vascular tissue anatomy of Norway spruce needles and twigs in relation to magnesium deficiency. Tree Physiol 13:337–349
Hanstein S, Wang XZ, Qian XQ, Friedhoff P, Fatima A, Shan YH, Feng K, Schubert S (2011) Changes in cytosolic Mg2+ levels can regulate the activity of the plasma membrane H+-ATPase in maize. Biochem J 435:93–101
Hariadi Y, Shabala S (2004) Screening broad beans (Vicia faba) for magnesium deficiency. II. Photosynthetic performance and leaf bioelectrical responses. Funct Plant Biol 31:539–549
Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Skrumsager Møller I, White P (2012) Functions of macronutrients. In: Marschner P (ed) Mineral nutrition of higher plants. Elsevier, Amsterdam, pp 135–189
Hermans C, Verbruggen N (2005) Physiological characterization of Mg deficiency in Arabidopsis thaliana. J Exp Bot 418:2153–2161
Hermans C, Jhonson GN, Strasser RJ, Verbruggen N (2004) Physiological characterization of magnesium deficiency in sugar beet: acclimation to low magnesium differentially affects photosystems I and II. Planta 220:344–355
Hermans C, Bourgis F, Faucher M, Strasser RJ, Delrot S, Verbruggen N (2005) Magnesium deficiency in sugar beets alters sugar partitioning and phloem loading in young mature leaves. Planta 220:541–549
Igamberdiev AU, Kleczkowski LA (2003) Membrane potential, adenylate levels and Mg2+ are interconnected via adenylate kinase equilibrium in plant cells. Biochim Biophys Acta 1607:111–119
Ivanov AG, Morgan R, Gray GR, Velitchkova MY, Huner NPA (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430:288–292
Ivanov AG, Hendrickson L, Krol M, Selstam E, Öquist G, Hurry V, Huner NPA (2006) Digalactosyl-diacylglycerol deficiency impairs the capacity for photosynthetic intersystem electron transport and state transitions in Arabidopsis thaliana due to photosystem I acceptor-side limitations. Plant Cell Physiol 47:1146–1157
Ivanov AG, Allakhverdiev SI, Huner NPA, Murata N (2012) Genetic decrease in fatty acid unsaturation of phosphatidylglycerol increased photoinhibition of photosystem I at low temperature in tobacco leaves. Biochim Biophys Acta 1817:1374–1379
Kaftan D, Brumfeld V, Nevo R, Scherz A, Reich Z (2002) From chloroplasts to photosystems: in situ scanning force microscopy on intact thylakoid membranes. EMBO J 21:6246–6253
Kanazawa S, Sano S, Koshiba T, Ushimaru T (2000) Changes in antioxidative in cucumber cotyledons during natural senescence: comparison with those during dark-induced senescence. Physiol Plant 109:211–216
Kehres DG, Maguire ME (2002) Structure, properties and regulation of magnesium transport proteins. Biometals 15:261–270
Klughammer C, Schreiber U (1991) Analysis of light-induced absorbancy changes in the near-infrared spectral region. 1: characterization of various components in isolated chloroplasts. Z Naturforsch C 46:233–244
Laing W, Greer D, Sun O, Beets P, Lowe A, Payn T (2000) Physiological impacts of Mg deficiency in Pinus radiata: growth and photosynthesis. New Phytol 146:47–57
Lasa B, Frechilla S, Aleu M, González-Moro B, Lamsfus C, Aparicio-Tejo PM (2000) Effects of low and high levels of magnesium on the response of sunflower plants grown with ammonium and nitrate. Plant Soil 225:167–174
Lavon R, Salomon R, Goldschmidt EE (1999) Effect of potassium, magnesium, and calcium deficiencies on nitrogen constituents and chloroplast components in Citrus leaves. J Am Soc Hortic Sci 124:158–162
Ling LL, Peng LZ, Cao L, Jiang CL, Chun CP, Zhang GY, Wang ZX (2009) Effect of magnesium deficiency on photosynthesis characteristic of Beibei 447 Jinchen orange. J Fruit Sci 26:275–280
Maguire ME, Cowan JA (2002) Magnesium chemistry and biochemistry. Biometals 15:203–210
Marschner H (2012) In: Marschner P (ed) Mineral nutrition of higher plants. Academic Press, London
Marschner H, Cakmak I (1989) High light intensity enhances chlorosis and necrosis in leaves of zinc, potassium and magnesium deficient bean (Phaseolus vulgaris) plants. J Plant Physiol 134:308–315
Mengel K, Kirkby EA (1987) Principles of plant nutrition. International Potash Institute, Switzerland, pp 481–492
Mengel K, Kirkby EA (2001) Principles of plant nutrition. Kluwer Academic Publishers, Dordrecht
Mengutay M, Ceylan Y, Kutman UB, Cakmak I (2013) Adequate magnesium nutrition mitigates adverse effects of heat stress on maize and wheat. Plant Soil 368:57–72
Mesić M, Kisić I, Bašić F, Butorac A, Zgorelec Ž, Gašpar I (2007) Losses of Ca, Mg and SO4 2− with drainage water at fertilization with different nitrogen rates. Agric Conspec Sci 72:53–58
Mikkelsen R (2010) Soil and fertilizer magnesium. Better. Crops 94:26–28
Narwal RP, Kumar V, Singh JP (1985) Potassium and magnesium relationship in cowpea (Vigna unguiculata (L.) Walp.). Plant Soil 86:129–134
Niu Y, Chai R, Liu L, Jin G, Liu M, Tang C, Zhang Y (2014) Magnesium availability regulates the development of root hairs in Arabidopsis thaliana (L.) Heynh. Plant Cell Environ 37:2795–2813
Ntsika G, Deltrot S (1986) Changes in apoplastic and intracellular leaf sugars induced by the blocking of export in Vicia faba. Physiol Plant 68:145–153
O’Dell RE, Rajakaruna N (2011) Intraspecific variation, adaptation, and evolution. In: Harrison SP, Rajakaruna N (eds) Serpentine: evolution and ecology of a model system. University of California Press, Berkeley, pp 97–137
Pakrasi H, Ogawa T, Bhattacharrya-Pakrasi M (2001) Transport of metals: a key process in oxygenic photosynthesis. In: Aro EM, Anderson B (eds) Regulation of photosynthesis. Kluwer, Dordrecht, pp 253–264
Papenfuß KH, Schlichting E (1979) Bestimmende Faktoren des Mg-Haushaltes von Böden in der Bundesrepublik Deutschland. Magnes Bull 1:12–14
Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400
Peaslee DE, Moss DN (1966) Photosynthesis in K and Mg-deficient maize (Zea mays) leaves. Soil Sci Soc Am Proc 30:220–223
Peuke AD, Jeschke WD, Hartung W (2002) Flows of elements, ions and abscisic acid in Ricinus communis and site of nitrate reduction under potassium limitation. J Exp Bot 53:241–250
Puech L, Mehne-Jakobs B (1997) Histology of magnesium deficient Norway spruce needles influenced by nitrogen source. Tree Physiol 17:301–310
Ridolfi M, Garrec JP (2000) Consequences of an excess Al and a deficiency in Ca and Mg for stomatal functioning and net carbon assimilation of beech leaves. Ann Forest Sci 57:209–218
Riga P, Anza M, Garbisu C (2005) Suitability of the antioxidative system as marker of magnesium deficiency in Capsicum annuum L. plants under controlled conditions. Plant Growth Regul 46:51–59
Rook F, Corke F, Card Munz G, Smith C, Bevan MW (2001) Impaired sucrose induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signaling. Plant J 26:421–433
Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014
Schachtschabel P (1954) Das pflanzenverfügbare Magnesium des Bodens und seine Bestimmung. J Plant Nutr Soil Sci 67:9–23
Schimanski C (1981) The influence of certain experimental parameters on the flux characteristics of Mg-28 on the case of barely seedlings grown in hydroculture. Landwirtsch Forsch 34:154–165
Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:309–323
Shaul O, Hilgemann DW, Almeida-Engler J, Van Montagu M, Inzé D, Galili G (1999) Cloning and characterization of a novel Mg2+/H+ exchanger. EMBO J 18:3973–3980
Silva IR, Smyth TJ, Carter TE, Rufty TW (2001) Altered aluminum root elongation inhibition in soybean genotypes in the presence of magnesium. Plant Soil 230:223–230
Sprengel C (1828) Von den Substanzen der Ackerkrume und des Untergrundes. Journal fur Tecnische und Okonomische Chemie 2:423–474
Stelzer R, Lehmann H, Krammer D, Luttge U (1990) X-Ray microprobe analysis of vacuoles of spruce needle mesophyll, endodermis and transfusion parenchyma cells at different seasons of the year. Bot Acta 103:415–423
Sun OJ, Payn TW (1999) Magnesium nutrition and photosynthesis in Pinus radiata: clonal variation and influence of potassium. Tree Physiol 19:535–540
Sun OJ, Gielen GTHP, Sands R, Smith CT, Thorn AJ (2001) Growth, Mg nutrition and photosynthetic activity in Pinus radiata: evidence that NaCl addition counteracts the impact of low Mg supply. Trees 15:335–340
Taiz L, Zeiger E (2010) Plant physiology. Sinauer Associates, Sunderland
Tan K, Keltjens WG, Findenegg R (1991) Role of magnesium in combination with liming in alleviating acid-soil stress with the aluminium-sensitive sorghum genotype CV323. Plant Soil 136:65–71
Tang N, Li Y, Chen LS (2012) Magnesium deficiency-induced impairment of photosynthesis in leaves of fruiting Citrus reticulata trees accompanied by up-regulation of antioxidant metabolism to avoid photo-oxidative damage. J Plant Nutr Soil Sci 175:784–793
Terry N, Ulrich A (1974) Effects of magnesium deficiency on the photosynthesis and respiration of leaves of sugar beet. Plant Physiol 54:379–381
Tewari RK, Kumar P, Tewari N, Srivastava S, Sharma PN (2004) Macronutrient deficiencies and differential antioxidant responses-influence on the activity and expression of superoxide dismutase in maize. Plant Sci 166:687–694
Tewari RK, Kumar P, Sharma PN (2006) Magnesium deficiency induced oxidative stress and antioxidant responses in mulberry plants. Sci Hort 108:7–14
Tisdale SL, Nelson WL, Beaton JD, Havlin JL (1993) Soil fertility and fertilisers. Prentice Hall, Upper Saddle River
Turner TL, Bourne EC, Von Wttberg EJ, Hu TT, Nuzhdin SV (2010) Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat Genet 42:260–263
Verbruggen N, Hermans C (2013) Physiological and molecular responses to magnesium nutritional imbalance in plants. Plant Soil 368:87–99
Vicić DD, Stoiljković MM, Bojat NČ, Sabovljević MS, Stevanović BM (2014) Physiological tolerance mechanisms of serpentine tolerant plants from Serbia. Rev Écol (Terre Vie) 69
Voogt W (1998) The growth of beefsteak tomato as affected by K/Ca ratios in the nutrient solution. Glasshouse Crops Research Station Naaldwijk, The Netherlands
Walker CJ, Weinstein JD (1991) Further characterization of the magnesium chelatase in isolated developing cucumber chloroplasts. Plant Physiol 95:1189–1196
White PJ (2012) Ion uptake mechanisms of individual cells and roots: short-distance transport. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants. Academic Press, London, pp 7–47
Wilkinson S, Welch R, Mayland H, Grunes D (1990) Magnesium in plants: uptake, distribution, function and utilization by man and animals. Metal Ions Biol Syst 26:33–56
Wingler A, Brownhill E, Pourtau N (2005) Mechanisms of the light-dependent induction of cell death in tobacco plants with delayed senescence. J Exp Bot 56:2897–2905
Yang GH, Yang LT, Jiang HX, Li Y, Wang P, Chen LS (2012) Physiological impacts of magnesium-deficiency in Citrus seedlings: photosynthesis, antioxidant system and carbohydrates. Trees 26:1237–1250
Zhang J, George E (2002) Changes in the extractability of cations (Ca, Mg and K) in the rhizosphere soil of Norway spruce (Picea abies) roots. Plant Soil 243:209–217
Zhao R, Dielen V, Kinet JM, Boutry M (2000) Cosupression of a plasma membrane H+-ATPase isoform impairs sucrose translocation, stomatal opening, plant growth and male fertility. Plant Cell 12:535–546
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A.K. Kononowicz.
Rights and permissions
About this article
Cite this article
Farhat, N., Elkhouni, A., Zorrig, W. et al. Effects of magnesium deficiency on photosynthesis and carbohydrate partitioning. Acta Physiol Plant 38, 145 (2016). https://doi.org/10.1007/s11738-016-2165-z
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-016-2165-z