Abstract
Magnesium deficiency in plants is a widespread problem, affecting productivity and quality in agriculture, yet at a physiological level it has been poorly studied in crop plants. Here, a physiological characterization of Mg deficiency in Beta vulgaris L., an important crop model, is presented. The impact of Mg deficiency on plant growth, mineral profile and photosynthetic activity was studied. The aerial biomass of plants decreased after 24 days of hydroponic culture in Mg-free nutrient solution, whereas the root biomass was unaffected. Analysis of mineral profiles revealed that Mg decreased more rapidly in roots than in shoots and that shoot Mg content could fall to 3 mg g−1 DW without chlorosis development and with no effect on photosynthetic parameters. Sucrose accumulated in most recently expanded leaves before any loss in photosynthetic activity. During the development of Mg deficiency, the two photosystems showed sharply contrasting responses. Data were consistent with a down-regulation of PSII through a loss of antenna, and of PSI primarily through a loss of reaction centres. In each case, the net result was a decrease in the overall rate of linear electron transport, preventing an excess of reductant being produced during conditions under which sucrose export away from mature leaf was restricted.
Similar content being viewed by others
Abbreviations
- Chl a, b:
-
Chlorophyll a, b
- DW :
-
Dry weight
- P700 :
-
Primary electron donor of photosystem I
- PSI, PSII:
-
Photosystem I, II
- Q A :
-
Primary quinone electron acceptor of PSII
- RC :
-
Reaction centre
References
Aitken RL, Dickson T, Hailes KJ, Moody PW (1999) Response of field-grown maize to applied magnesium in acidic soil in north-eastern Australia. Aust J Agric Res 50:191–198
Amalou Z, Gibrart R, Trouslot P, d’Auzac J (1994) Solubilization and reconstitution of the Mg2+/2H+ antiporter of the lutoid tonoplast from Hevea brassiliensis latex. Plant Physiol 106:79–85
Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60:43–73
Bennett WF (1997) Nutrients deficiencies & toxicities in crop plants. APS Press, The American Phythopathological Society, St. Paul, MN, USA
Blair JM (1970) Magnesium, potassium and the adenylate kinase equilibrium. Magnesium as a feedback signal from the adenine nucleotide pool. Eur J Biochem 13:384–390
Bui DM, Gregan J, Jarosch E, Ragnini A, Schweyen JR (1999) The bacterial magnesium transporter CorA can functionally substitute for its putative homologue Mrsp2p in the yeast inner mitochondrial membrane. J Biol Chem 274:20438–20443
Butler WL, Kitajima M (1975) Fluorescence quenching in photosystem II of chloroplasts. Biochim Biophys Acta 376:116–125
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
Clarke JE, Johnson GN (2001) In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 212:808–816
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
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 Plant 89:271–276
Fischer ES, Lohaus G, Heineke D, Heldt HW (1998) Magnesium deficiency results in accumulation of carbohydrates and amino acids in source and sink leaves of spinach. Physiol Plant 102:16–20
Foyer CH (1988) Feedback inhibition of photosynthesis through source–sink regulation in leaves. Plant Physiol Biochem 26:483–492
Gardner RC (2003) Genes for magnesium transport. Curr Opin Plant Biol 6:263–267
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
Ghoulam C, Foursy A, Fares K (2002) Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ Exp Bot 47:39–50
Golding A, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114
Hermans C, Smeyers M, Rodriguez RM, Eyletters M, Strasser RJ, Delhaye JP (2003). Quality assessment of urban trees: a comparative study of physiological characterisation, airborne imaging and on site fluorescence monitoring by the OJIP-test. J Plant Physiol 160:81–90
Igamberdiev AU, Kleczkowski LA (2001) Implications of adenylate kinase-governed equilibrium of adenylates on contents of free magnesium in plant cells and compartments. Biochem J 360:225–231
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
Jensen PE, Haldrup A, Rosgaard L, Scheller HV (2003) Molecular dissection of photosystem I in higher plants: topology, structure and function. Physiol Plant 119:313–321
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
Kehres DG, Maguire ME (2002) Structure properties and regulation of magnesium transport proteins. Biometals 15:261–270
Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115
Klughammer C, Schreiber U (1991) Analysis of light-induced absorbance changes in the near-infrared spectral region. I. Characterization of various components in isolated chloroplasts. Z Naturforsch Teil C 46:233–244
Kramer DM, Crofts AR (1996) Control and measurement of photosynthetic electron transport in vivo. In: Baker NR (ed.) Advances in photosynthesis: environmental stress and photosynthesis. Kluwer, Dordrecht, pp 25–66
Laing W, Greer D, Sun O, Beets P, Lowe, Payn T (2000) Pysiological impacts of Mg deficiency in Pinus radiata: growth and photosynthesis. New Phytol 146:47–57
Lasa B, Freschilla 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
Li L, Tutone AF, Drummond RSM, Gardner RC, Luan S (2001) A novel family of magnesium transport genes in Arabidopsis. Plant Cell 13:2761–2775
López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287
Lu Y-K, Chen Y-R, Yang C-M (1995) Influence of Fe- and Mg-deficiency on the thylakoid membranes of a chlorophyll-deficient ch5 mutant of Arabidopsis thaliana. Bot Bull Acad Sin 36:175–179
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London
Marschner H, Kirkby EA, Cakmak I (1996) Effect of mineral nutritional status on shoot–root partitioning of photoassimilates and cycling of mineral nutrients. J Exp Bot 47:1255–1263
Mehne-Jakobs B (1995) The influence of magnesium deficiency on carbohydrate concentrations in Norway spruce (Picea abies) needles. Tree Physiol 15:577–584
Mengel K, Kirkby EA (1987) Principles of plant nutrition, 4th edn. International Potash Institute, Worblaufen-Bern, Switzerland, pp 481–492
Mitchell AD, Loganathan P, Payn TW, Tillman RW (1999) Effect of calcined magnesite on soil and Pinus radiata foliage magnesium in pumice soils of New Zealand. Aust J Soil Res 37:545–560
Oswald O, Martin T, Dominy PJ, Graham IA (2001) Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA 98:2047–2052
Ott T, Clarke J, Birks K, Johnson GN (1999) Regulation of the photosynthetic electron transport chain. Planta 209:250–258
Paillotin G (1976) Movement of excitations in the photosynthesis domain of photosystem II. J Theor Biol 58:237–252
Pakrasi H, Ogawa T, Bhattacharrya-Pakrasi M (2001) Transport of metals: a key process in oxygenic photosynthesis. In: Aro E-M, Anderson B (eds) Regulation of photosynthesis. Kluwer, Dordrecht, pp 253–264
Pate JS, Shedley E, Arthur D, Adams MA (1998) Spatial and temporal variations in phloem sap composition of plantation-grown Eucalyptus globules. Oecologia 117:312–322
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
Pfeiffer W, Hager A (1993) A Ca2+-ATPase and a Mg2+/H+-antiporter are present on tonoplast membranes from roots of Zea mays L. Planta 191:377–385
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectrometry. Biochim Biophys Acta 975:384–394
Pujos A, Morard P (1997) Effects of potassium deficiency on tomato growth and mineral nutrition at the early production stage. Plant Soil 189:189–196
Rychter AM, Chauveau M, Bomsel J-L, Lance C (1992) The effect of phosphate deficiency on mitochondrial activity and adenylate levels in bean roots. Physiol Plant 84:80–86
Schock I, Gregan J, Steinhauser S, Schweyen R, Brennicke A, Knoop V (2000) A member of a novel Arabidopsis thaliana gene family of candidate Mg2+ ion transporters complements a yeast mitochondrial group II intron-splicing mutant. Plant J 24:489–501
Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:309–323
Shaul O, Hilgemann DW, Aldmeida-Engler J, Van Montagu M, Inzé D, Galili G (1999) Cloning and characterization of a novel Mg2+/H+ exchanger. EMBO J 18:3973–3980
Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038
Sokolov LN, Déjardin A, Kleczkowski LA (1998) Sugars and light/dark exposure trigger differential regulation of ADP-glucose pyrophosphorylase genes in Arabidopsis thaliana (thale cress). Biochem J 336:681–687
Srivastava A, Strasser RJ, Govindjee (1999) Greening of peas: parallel measurements of 77 K emission spectra, OJIP chlorophyll a fluorescence transient, period for oscillation of the initial fluorescence level, delayed light emission, and P700. Photosynthetica 37:365–392
Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. J Photochem Photobiol 61:32–42
Sun OJ, Gielen GJHP, Tattersall Smith RSC, Thorn AJ (2001) Growth, Mg nutrition and photosynthetic activity of Pinus radiata: evidence that NaCl addition counteracts the impact of low Mg supply. Trees 15:335–340
Surpin M, Larkin RM, Chory J (2002) Signal transduction between the chloroplast and the nucleus. Plant Cell [Suppl] 14:327–338
Terry N, Ulrich A (1974) Effects of magnesium deficiency on the photosynthesis and respiration of leaves of sugar beet. Plant Physiol 54:379–381
Weis E, Lechtenberg D (1989) Fluorescence analysis during steady-state photosynthesis. Philos Trans R Soc Lond Ser B 323:253–268
Wilkinson SR, Welch RM, Mayland HF, Grunes DL (1990) Magnesium in plants: uptake, distribution, function and utilization by man and animals. Metal Ions Biol Syst 26:33–56
Wingler A, Mares M, Pourtau N (2004) Spatial patterns and metabolic regulation of photosynthetic parameters during leaf senescence. New Phytol 161:781–789
Wu W, Peters J, Berkowitz GA (1991) Surface charge-mediated effects of Mg2+ on K+ flux across the chloroplast envelope are associated with regulation of stromal pH and photosynthesis. Plant Physiol 97:580–587
Acknowledgements
C. Hermans was supported by a grant from Fonds pour la Formation de la Recherche dans l’Industrie et dans l’Agriculture. This research was supported by grant from the Interuniversity Attraction Pole Program—Belgian Science Policy (Project V/13). Part of the experimental work was done during a Marie Curie Studentship Training Site program at the Biological School of The University of Manchester. Access to the spectrometer equipment was provided by Prof. C. Buess, Laboratoire de Chimie Analytique, Université Libre de Bruxelles.
Author information
Authors and Affiliations
Corresponding author
Appendix: definition of photosynthetic parameters
Appendix: definition of photosynthetic parameters
PSII fluorescence parameters
Maximum quantum yield for primary photochemistry at time zero
(Butler and Kitajima 1975; Kitajima and Butler 1975)
Actual quantum yield for primary phytochemistry at time t
(Paillotin 1976)
where relative variable fluorescence at the state t is given by Vt=(Ft−FO)/(FM−FO)
Actual quantum yield for primary photochemistry at steady state under a given light condition
(Genty et al. 1989)
where ′ refers to the light-adapted state, and relative variable fluorescence at the various states is given by VS′=(FS′−FO′)/(FM′−FO′).
Rate of electron transport
Performance index (PI) and driving force (DF) of PSII
(Hermans et al. 2003)
where:
PSI absorbance parameters
Maximum signal amplitude induced by far-red light on dark-adapted leaves
(Weis and Lechtenberg 1989)
Signal amplitude following a light-to-dark transition on light-adapted leaves
(Weis and Lechtenberg 1989)
Rate of PSI electron transport calculated on a total P700 basis
(Clark and Johnson 2001)
Rate of PSI electron transport per P700 oxidised fraction
(Ott et al. 1999)
where k is the rate constant for P700 re-reduction.
Rights and permissions
About this article
Cite this article
Hermans, C., Johnson, G.N., Strasser, R.J. et al. Physiological characterisation of magnesium deficiency in sugar beet: acclimation to low magnesium differentially affects photosystems I and II. Planta 220, 344–355 (2004). https://doi.org/10.1007/s00425-004-1340-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-004-1340-4