Skip to main content
SpringerLink
Log in

Preferential damaging effects of limited magnesium bioavailability on photosystem I in Sulla carnosa plants

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Magnesium deficiency preferentially inhibits photosystem I rather than photosystem II in Sulla carnosa plants.

The effects of magnesium (Mg2+) deficiency on growth, photosynthetic performance, pigment and polypeptide composition of chloroplast membranes were studied in the halophyte Sulla carnosa (Desf.), an annual legume endemic to Tunisia and Algeria. The results demonstrate a gradual decrease in biomass production with decreasing Mg2+ availability in the growth medium. The increase of Mg2+ deficiency was also associated with a decline of the net CO2 assimilation (Pn) in fully expanded leaves, a decrease in the amount of photosynthetic pigments, and an increase in the lipid peroxidation in plants exposed to decreased Mg2+ concentrations. Interestingly, while CO2 assimilation already was affected at Mg2+ concentrations below 1.5 mM, the photochemical efficiency of photosystem II (PSII) declined only in the absence of Mg2+. In contrast, plants of S. carnosa grown in Mg2+-deficient conditions exhibited a significant decrease in photosystem I (PSI) photochemistry in vivo at much higher Mg2+ levels compared to PSII photochemical activity. The inhibitory effect of Mg2+ deficiency on PSI photochemistry strongly correlated with significantly lower relative abundance of PSI-related chlorophyll–protein complexes and lower amounts of PSI-associated polypeptides, PsaA, PsaB, and Lhca proteins within the same range of Mg2+ concentrations. These observations were associated with a higher intersystem electron pool size, restricted linear electron transport and a lower rate of reduction of P700+ in the dark indicating restricted capacity for PSI cyclic electron transfer in plants exposed to Mg2+-deficient conditions compared to controls. These results clearly indicate that PSI, rather than PSII is preferentially targeted and damaged under Mg2+-deficiency conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

AL:

Actinic light

Car:

Carotenoids

Chl:

Chlorophyll

C i :

Intercellular CO2 concentration

E :

Transpiration

ETR:

Electron transport rate

F m :

Maximal chlorophyll fluorescence in dark-adapted state

\( F_{\text{m}}^{\prime } \) :

Maximal chlorophyll fluorescence in light-adapted state

F o :

Minimal chlorophyll fluorescence in dark-adapted state

\( F_{\text{o}}^{\prime } \) :

Minimal chlorophyll fluorescence in light-adapted state

F v :

Variable chlorophyll fluorescence in dark-adapted state

F v/F m :

Maximal quantum efficiency of PSII

ΦPSII :

Effective quantum yield of PSII electron transport

FR:

Far-red

gs:

Stomatal conductance

MDA:

Malonyldialdehyde

MT:

Multiple-turnover flash

qN:

Non-photochemical quenching coefficient

qP:

Photochemical quenching coefficient

P700:

Reaction center pigment of PSI

P700+ :

Oxidized form of the reaction center of PSI

PAR:

Photosynthetically active radiation

Pn:

Net CO2 assimilation

PS:

Photosystem

ST:

Single-turnover flash

WUE:

Water use efficiency

References

  • Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59:1555–1568

    CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    PubMed Central  CAS  PubMed  Google Scholar 

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    CAS  PubMed  Google Scholar 

  • Asada K, Heber U, Schreiber U (1992) Pool size of electrons that can be donated to P700+, as determined in intact leaves: donation to P700+ from stromal components via the intersystem chain. Plant Cell Physiol 33:927–932

    CAS  Google Scholar 

  • Asada K, Heber U, Schreiber U (1993) Electron flow to the intersystem chain from stromal components and cyclic electron flow in maize chloroplasts, as determined in intact leaves by monitoring redox change of P700 and chlorophyll fluorescence. Plant Cell Physiol 34:39–50

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Barber J (1982) Influence of surface charge on thylakoid structure and functions. Annu Rev Plant Physiol 33:261–695

    CAS  Google Scholar 

  • Baszyński T, Brand J, Barr R, Krogmann DW, Crane FL (1972) Some biochemical characteristics of chloroplasts from mineral-deficient maize. Plant Physiol 50:410–411

    PubMed Central  PubMed  Google Scholar 

  • Baszyński T, Warchołowa M, Krupa Z, Tukendorf A, Król M, Wolińska D (1980) The effect of magnesium deficiency on photochemical activities of rape and buckwheat chloroplasts. Z Pflanzenphysiol 99:295–303

    Google Scholar 

  • Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60:43–73

    CAS  Google Scholar 

  • Bell LW, Lloyd DL, Bell KL, Johnson B, Teasdale KC (2003) First year and softening in three Hedysarum ssp. In southern Queensland. Aust J Exp Agric 43:1303–1310

    Google Scholar 

  • Bewick V, Cheek L, Ball J (2004) Statistics review 9: one-way analysis of variance. Crit Care 8(2):130–136

    PubMed Central  PubMed  Google Scholar 

  • Bolan NS, Loganathan P, Saggar S (2005) Calcium and magnesium in soils. Elsevier, Amsterdam

    Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2013) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot. doi:10.1093/jxb/ert430

    Google Scholar 

  • Cakmak I (2000) Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol 146:185–205

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cakmak I, Yazici AM (2010) Magnesium: a forgotten element in crop production. Better Crops 94:23–25

    Google Scholar 

  • Cakmak I, Hengeler C, Marschner H (1994) 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ceppi MG, Oukarroum A, Çiçek N, 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

    CAS  PubMed  Google Scholar 

  • Cowan JA (2002) Structural and catalytic chemistry of magnesium dependent enzymes. Biometals 15:225–235

    CAS  PubMed  Google Scholar 

  • Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128:379–387

    PubMed Central  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WWIII (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626

    CAS  Google Scholar 

  • Dobrikova A, Morgan RM, Ivanov AG, Apostolova E, Petkanchin I, Huner NPA, Taneva SG (2000) Electric properties of thylakoid membranes from pea mutants with modified carotenoid and chlorophyll–protein complex composition. Photosynth Res 65:165–174

    CAS  PubMed  Google Scholar 

  • Eaton TE-J, Cox DA, Barker AV (2012) Relationship of iron-manganese toxicity disorder in marigold to manganese and magnesium nutrition. J Plant Nutr 35:142–164

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Farhat N, Rabhi M, Krol M, Barhoum, 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 (accepted for publication)

  • Fischer ES (1997) Photosynthetic irradiance curves of Phaseolus vulgaris under moderate or severe magnesium deficiency. Photosynthetica 33:385–390

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 Plant 102:16–20

    CAS  Google Scholar 

  • Foy CD, Chaney RL, White MC (1978) The physiology of metal toxicity in plants. Annu Rev Plant Physiol 29:511–567

    CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Guller L, Krucka M (1993) Ultrastructure of grape-vine (Vitis vinifera) chloroplasts under Mg- and Fe-deficiency. Photosynthetica 29:417–425

    CAS  Google Scholar 

  • Hall JD, Bar R, Al-Abbas AH, Crane FL (1972) Ultrastructure of chloroplasts in mineral-deficient maize leaves. Plant Physiol 50:404–409

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Harrison HC, Bergman EL (1981) Calcium, magnesium, and potassium interrelationships affecting cabbage production. J Am Soc Hort Sci 106:500–503

    CAS  Google Scholar 

  • Herbert SK, Martin RE, Fork DC (1995) Light adaptation of cyclic electron transport through photosystem I in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res 46:277–285

    CAS  PubMed  Google Scholar 

  • Hermans C, Verbruggen N (2005) Physiological characterization of Mg deficiency in Arabidopsis thaliana. J Exp Bot 418:2153–2161

    Google Scholar 

  • Hermans C, Johnson 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hermans C, Vuylsteke M, Coppens F, Cristescu SM, Harren FJM, Inzé D, Verbruggen N (2010) Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. New Phytol 187:132–144

    CAS  PubMed  Google Scholar 

  • Hernandez JA, Almansa MS (2002) Short-term effects of salt stress on anti-oxidant systems and leaf water relations of pea leaves. Physiol Plant 115:251–257

    CAS  PubMed  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonw Bur Hort Tech Commun 22:431–446

    Google Scholar 

  • Horst WJ, Marschner H (1990) Mineral nutrition of higher plants. Academic Press, Boston

    Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    CAS  PubMed  Google Scholar 

  • Hu Y, Schmidhalter U (2001) Effect of salinity and macronutrient levels on micronutrients in wheat. J Plant Nutr 24:273–281

    CAS  Google Scholar 

  • Huner NPA, Maxwell DP, Gray GR, Savitch LV, Krol M, Ivanov AG, Falk S (1996) Sensing environmental change: PSII excitation pressure and redox signalling. Physiol Plant 98:358–364

    CAS  Google Scholar 

  • Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230

    Google Scholar 

  • Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M (2003) Early light-induced proteins protect Arabidopsis from photooxidative stress. Proc Natl Acad Sci USA 100:4921–4926

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ivanov AG, Sane PV, Hurry V, Öquist G, Huner NPA (2008) Photosystem II reaction centre quenching: mechanisms and physiological role. Photosynth Res 98:565–574

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Izawa S, Good NE (1966) Effect of salt and electron transport on the conformation of isolated chloroplasts. II. Electron microscopy. Plant Physiol 41:544–552

    CAS  Google Scholar 

  • Jithesh M-N, Prashanth S-R, Sivaprakash K-R, Parida A-K (2006) Antioxidative response mechanisms in halophytes: their role in stress defence. J Genet 85:237–254

    CAS  PubMed  Google Scholar 

  • Klughammer C, Schreiber U (1991) Analysis of light-induced absorbency changes in the near-infrared spectral region. 1. Characterization of various components in isolated chloroplasts. Z Naturforsch C 46:233–244

    CAS  Google Scholar 

  • Kosová K, Vítámvás P, Urban MO, Prášil I-T (2013) Plant proteome responses to salinity stress—comparison of glycophytes and halophytes. Funct Plant Biol 40:775–786

    Google Scholar 

  • Krol M, Ivanov AG, Jansson S, Kloppstech K, Huner NPA (1999) Greening under high light and cold temperature affects the level of xanthophyll-cycle pigments, early light-inducible proteins, and light harvesting polypeptides in wild-type barley and the Chlorina f2 mutant. Plant Physiol 120:193–203

    PubMed Central  CAS  PubMed  Google Scholar 

  • Laemmli U (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Lichlenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Google Scholar 

  • Lin DC, Nobel PS (1971) Control of photosynthesis by Mg2+. Arch Biochem Biophys 145:622–632

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–642

    CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press Inc., London

    Google Scholar 

  • Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by turnover of P700 in vivo. Biochemistry 15:3975–3981

    CAS  PubMed  Google Scholar 

  • Mengel K, Kirkby EA (1987) Principles of plant nutrition, 4th edn. International Potash Institute, Worblaufen-Bern, Switzerland, pp 481–492

    Google Scholar 

  • Mi H, Endo T, Schreiber U, Asada K (1992a) Donation of electrons from cytosolic components to the intersystem chain in the cyanobacterium Synechococcus sp. PCC 7002 as determined by the reduction of P700+. Plant Cell Physiol 33:1099–1105

    CAS  Google Scholar 

  • Mi H, Endo T, Schreiber U, Ogawa T, Asada K (1992b) Electron donation from cyclic and respiratory flows to the photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 33:1233–1237

    CAS  Google Scholar 

  • Millaleo R, Reyes-Díaz M, Alberdi M, Ivanov AG, Krol M, Hüner NPA (2013) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J Exp Bot 64:343–354

    PubMed Central  CAS  PubMed  Google Scholar 

  • Munekage Y, Hoja M, Meurer J, Endo T, Tasaka M, Shikamai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371

    CAS  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2005) Inhibition of the repair of PSII by oxidative stress in cyanobacteria. Photosynth Res 84:1–7

    CAS  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749

    CAS  PubMed  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359

    CAS  PubMed  Google Scholar 

  • Ojakian G, Satir P (1974) Particle movements in chloroplast membranes: quantitative measurements of membrane fluidity by the freeze-fracture technique. Proc Natl Acad Sci USA 71:2052–2065

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ozgur R, Uzilday B, Sekmen A-H, Turkan I (2013) Reactive oxygen species regulation and antioxidant defence in halophytes. Funct Plant Biol 40:832–847

    CAS  Google Scholar 

  • Peaslee DE, Moss DN (1966) Photosynthesis in K and Mg-deficient maize (Zea mays) leaves. Soil Sci Soc Am Proc 30:220–223

    CAS  Google Scholar 

  • Peng Y, Lin W, Wei H, Krebs SL, Arora R (2008) Phylogenetic analysis and seasonal cold acclimation-associated expression of early light-induced protein genes of Rhododendron catawbiense. Physiol Plant 132:44–52

    CAS  PubMed  Google Scholar 

  • Pérez V, Wherrett T, Shabala S, Muñiz J, Dobrovinskaya O, Pottosin I (2008) Homeostatic control of slow vacuolar channels by luminal cations and evaluation of the channel-mediated tonoplast Ca2+ fluxes in situ. J Exp Bot 59:3845–3855

    PubMed Central  PubMed  Google Scholar 

  • Quézel P, Santa S (1962–1963) Nouvelle Flore de l’Algérie et des Régions Désertiques Méridionales. Paris: Éditions du Centre National de la Recherche Scientifique

  • Rafter JA, Abell ML, Braselton JP (2002) Multiple comparison methods for means. SIAM Rev 44(2):259–278

    Google Scholar 

  • Ravenel J, Peltier G, Havaux M (1994) The cyclic electron pathways around photosystem I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage. Planta 193:251–259

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Savitch LV, Ivanov AG, Krol M, Sprott DP, Öquist G, Huner NPA (2010) Regulation of energy partitioning and alternative electron transport pathways during cold acclimation of Lodgepole pine is oxygen dependent. Plant Cell Physiol 51:1555–1570

    CAS  PubMed  Google Scholar 

  • Scheller H, Haldrup A (2005) Photoinhibition of photosystem I. Planta 221:5–8

    CAS  PubMed  Google Scholar 

  • Schreiber U (1994) New emitter-detector-cuvette assembly for measuring modulated chlorophyll fluorescence of highly diluted suspensions in conjunctions with the standard PAM fluorometer. Z Naturforsch C 49:646–656

    CAS  Google Scholar 

  • Shabala S, Shabala L, Van Volkenburgh E, Newman I (2005) Effect of divalent cations on ion fluxes and leaf photochemistry in salinized barley leaves. J Exp Bot 415:1369–1378

    Google Scholar 

  • Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:309–323

    CAS  PubMed  Google Scholar 

  • Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 10:8827–8832

    Google Scholar 

  • Sonoike K, Kamo M, Hihara Y, Hiyama T, Enami I (1997) The mechanism of the degradation of PsaB gene product, one of the photosynthetic reaction centre subunits of photosystem I, upon photoinhibition. Photosynth Res 53:55–63

    CAS  Google Scholar 

  • Stienezen M, Waghorn GC, Douglas GB (1996) Digestibility and effects of condensed tannins on digestion of Sulla (Hedysarum coronarium) when fed to sheep. N Z Agric Res 39:215–221

    Google Scholar 

  • Sun OJ, Payn TW (1999) Magnesium nutrition and photosynthesis in Pinus radiata: clonal variation and influence of potassium. Tree Physiol 19:535–540

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Takahashi S, Milward SE, Fan DY, Chow WS, Badger MR (2009) How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiol 149:1560–1567

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tang N, Li Y, Chen L-S (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

    CAS  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN (2006) Magnesium deficiency induced oxidative stress and antioxidant responses in mulberry plants. Sci Hort 108:7–14

    Google Scholar 

  • Thomas PG, Quinn PJ, Williams WP (1986) The origin of photosystem I-mediated electron transport stimulation in heat-stressed chloroplasts. Planta 167:133–139

    CAS  PubMed  Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    PubMed Central  CAS  PubMed  Google Scholar 

  • Verbruggen N, Hermans C (2013) Physiological and molecular responses to magnesium nutritional imbalance in plants. Plant Soil 368:87–99

    CAS  Google Scholar 

  • Whatley JA (1971) Ultrastructural changes in chloroplasts of Phaseolus vulgaris during development under conditions of nutrient deficiency. New Phytol 70:725–742

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Williams L, Salt DE (2009) The plant ionome coming into focus. Curr Opin Plant Biol 12:247–249

    PubMed Central  CAS  PubMed  Google Scholar 

  • Woodgate K, Maxted N, Bennett SJ (1999) A genetic conspectus of the forage legumes of the Mediterranean basin. In: Bennett SJ, Cocks PS (eds) Genetic resources of Mediterranean pasture and forage legumes. Kluwer Academic Publishers, London, pp 194–195

    Google Scholar 

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

    CAS  Google Scholar 

  • Yu Q, Rengel Z (1999) Micronutrient deficiency influences plant growth and activities of superoxide dismutases in narrow-leafed lupins. Ann Bot 83:175–182

    CAS  Google Scholar 

  • Yu L, Zhao L, Muhlenhoff U, Bryant DA, Golbeck JH (1993) PsaE is required for in vivo cyclic electron flow around photosystem I in the cyanobacterium Synechococcus sp. PCC 7002. Plant Physiol 103:171–180

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yu Q, Osborne LD, Rengel Z (1999) Increased tolerance to Mn deficiency in transgenic tobacco overproducing superoxide dismutase. Ann Bot 84:543–547

    CAS  Google Scholar 

  • Yu-Chuan D, Chun-Rong C, Wen L, Yan-Shou W, Xiao-Li R, Ping W, Guo-Hua X (2008) High potassium aggravates the oxidative stress induced by magnesium deficiency in rice leaves. Pedosphere 18:316–327

    Google Scholar 

  • Zarter CP, Adams WWIII, Ebbert V, Cuthberson DJ, Adamska I, Demmig-Adams B (2006) Winter down-regulation of intrinsic photosynthetic capacity coupled with up-regulation of Elip-like proteins and persistent energy dissipation in a subalpine forest. New Phytol 172:271–282

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Tunisian Ministry of Higher Education and Scientific Research (LR10CBBC02) and the Natural Science and Engineering Research Council of Canada to Professor Norman P.A. Huner, Department of Biology, University of Western Ontario.

Author information

Authors and Affiliations

  1. Laboratory of Extremophile Plants, Biotechnology Centre of Borj-Cedria, P. O. Box 901, 2050, Hammam-Lif, Tunisia

    Nèjia Farhat, Mokded Rabhi, Abderrazak Smaoui & Chedly Abdelly

  2. Department of Biology, University of Western Ontario, 1151 Richmond Street N., London, ON, N6A 5B7, Canada

    Alexander G. Ivanov, Marianna Krol & Norman P. A. Hüner

Authors
  1. Nèjia Farhat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander G. Ivanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marianna Krol
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mokded Rabhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abderrazak Smaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chedly Abdelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Norman P. A. Hüner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander G. Ivanov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Farhat, N., Ivanov, A.G., Krol, M. et al. Preferential damaging effects of limited magnesium bioavailability on photosystem I in Sulla carnosa plants. Planta 241, 1189–1206 (2015). https://doi.org/10.1007/s00425-015-2248-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-015-2248-x

Keywords

Search

Navigation