Abstract
Lanthanoids (Ln) were demonstrated to improve chlorophyll formation and the growth of plants. But the mechanism of the fact that Ln promotes chlorophyll biosynthesis of plants is poorly understood. The main aim of the study was to determine Ln effects in chlorophyll formation of maize under magnesium (Mg) deficiency. Maize plants were cultivated in Hoagland’s solution. They were subjected to Mg deficiency and to cerium administered in Mg-deficient Hoagland’s media, and then the contents of various chlorophyll precursors and gen expressions of the key enzymes of chlorophyll biosynthesis were examined. The decrease of chlorophyll contents in maize leaves caused by Mg deficiency suggested an inhibition of chlorophyll synthesis that was inhibited by a reduction of the precursors as measured by analyzing the contents of δ-aminolevulinic acid, porphobilinogen, uroporphyrinogen III, Mg–protoporphyrin IX, and protochlorophyll, as well as the expression levels of magnesium chelatase, magnesium-protoporphyrin IX methyltransferase, and chlorophyll synthase; Mg deficiency significantly inhibited the transformation from coproporphyrinogen III or protoporphyrin IX to chlorophyll. However, cerium addition significantly relieved the inhibition of chlorophyll biosynthesis in maize caused by Mg deficiency and increased chlorophyll content and promoted a series of transformations from δ-aminolevulinic acid to chlorophyll and maize growth under Mg deficiency. It implied that cerium might partly substitute for the role of Mg.
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References
Von Wettstein D, Gough S, Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7:1039–1057
Porra RJ (1997) Recent process in porphyrin and chlorophyll biosynthesis. Photochem Photobiol 65:492–516
Gopal K, Pattanayak GK, Biswal AK, Reddy VS, Tripathy BC (2005) Light-dependent regulation of chlorophyll b biosynthesis in chlorophyllide a oxygenase overexpressing tobacco plants. Biochemd Biophys Res Commun 326:466–471
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London
Buchanan BB, Gruissem W, Johones RL (2002) Biochemistry and molecular biology of plants. American Society of Plant Physiology, Science Press, Beijing, pp 568–628
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
Woodward RB, Ayer WA, Beaton JM, Bickelhaupt F, Bonnett R, Buchschacher P, Closs GL, Dutler H, Hannah J, Hauck FP, Shŏ I, Langemann A, Goff EL, Leimgruber W, Lwowski W, Sauer J, Valenta Z, Volz H (1990) The total synthesis of chlorophyll a. Tetrahedron 46(22):7599–76598
Speer and Brian R (1997) Photosynthetic Pigments in UCMP glossary (online). University of California, Berkeley Museum of Paleontology. Verified availability March 12, 2007
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
Balakrishnan K, Rajendran C, Kulandaivelu G (2000) Differential responses of iron, magnesium, and zinc deficiency on pigment composition, nutrient content, and photosynthetic activity in tropical fruit crops. Photosynthetica 38(3):477–479
Santos CV (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hortic 103:93–99
Liao TJ, Huang Y, Su BY (1994) Study of REEs on yield, quality and physiological effect of spinach. Chinese Rare Earths 15(5):26–29
Chu ZX, Mu MH, Shao HX (1994) Influences of Ce3+ on the formation of chlorophyll–protein complexes in chloroplasts of cucumber leaves. Acta Bot Sin 36(10):785–789
Hong FS, Wei ZG, Zhao GW (2002) Mechanism of lanthanum effect on the chlorophyll of spinach. Sci China Ser C 45(2):166–176
Hong FS, Wang L, Meng XX, Wei ZG, Zhao GW (2002) The effect of cerium on the chlorophyll formation of spinach. Biol Trace Element Res 89:263–277
Hong FS, Wang XF, Liu C, Su GX, Song WP, Wu K, Tao Y, Zhao GW (2003) Effect of Ce3+ on spectral characteristic of D1/D2/Cytb559 complex from spinach. Sci China B 46(1):42–49
Yin ST, Ze YG, Liu C, Li N, Zhou M, Duan YM, Hong FS (2009) Cerium relieves the inhibition of nitrogen metabolism of spinach caused by magnesium deficiency. Biol Trace Element Res 132(1–3):247–258
Meider H (1984) Class experiments in plant physiology. Allen and Unwin, London, pp 72–74
Hong FS, Fang NH, Zhao GW (2000) Physiological effects of cerium nitrate on seed germination of rice. Acta Agronomica Sinica 26(1):7–12 (in Chinese)
Hong FS (2002) Study on the mechanism of cerium nitrate effects on germination of aged rice seed. Biol Trace Elem Res 87:191–200
Liu C, Hong FS, Zheng L, Tang P, Wang ZG (2004) Effects of rare earth elements on vigor enhancement of aged spinach seeds. J Rare Earths 22(4):547–552
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15
Porra JR (1990) The extraction and assay of refractory chlorophylls and a simple method to correct data from Arnon’s equations. Curr Res Photosyn 11:237–240
Dei M (1985) Benzyladenine-induced stimulation of δ-aminolevulinic acid accumulation under various light intensities in levulinic acid-treated cotyledons of etiolated cucumber. Physiol Plant 64:153–160
Bogora L (1962) Porphyrin synthesis. In: Colowick SP, Kaplan NO (eds) Methods in enzymology, vol 5. Academic, New York, pp 885–891
Rebeiz CA, Mattheis JR, Smith BB, Rebeiz CC, Dayton DF (1975) Chloroplast biogenesis and accumulation of protochlorophyll by isolated etioplasts and developing chloroplasts. Arch Biochem Biophys 171:549–56727
Lee HJ, Ball MD, Parham R, Rebeiz CA (1992) Chloroplast biogenesis 65 enzymic conversion of protoporphyrin IX to Mg–protoporphyrin IX in a subplastidic membrane fraction of cucumber etiochloroplasts. Plant Physiol 99:1134–1140
Ke LD, Chen Z (2000) A reliability test of standard-based quantitative PCR: exogenous vs endogenous standards. Mol Cell Probes 14(2):127–135
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408
Liu WH, David A (2002) Saint validation of a quantitative method for real time PCR kinetics. Biochem Biophys Res Commun 294:347–353
Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60:43–73
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
Cowan JA (2002) Structural and catalytic chemistry of magnesium dependent enzymes. Biometals 15:225–235
Polle A, Otter T, Mehne-Jakobs B (1994) Effect of magnesium-deficiency on antioxidative systems in needles of Norway spruce (Picea abies (L.) Karst.) grown with different ratios of nitrate and ammonium as nitrogen sources. New Phytol 128:621–628
Anza M, Riga P (2001) Effect of magnesium deficiency in antioxidant enzymes from pepper plants (Capsicum annuum L.). Acta Hortic 559:365–370
Cakmak I (1994) Activity of ascorbate-dependent H2O2-scavenging enzymes and leaf chlorosis are enhanced in magnesium and potassium deficient leaves, but not in phosphorus-deficient leaves. J Exp Bot 45(278):1259–1266
Hermans C, Johnson GN, Strasser RJ, Verbruggen N (2004) Physiological characterisation of magnesium deficiency in sugar beet: acclimation to low magnesium differentially affects photosystems I and II. Planta 220:344–355
Fang Z, Bouwkamp J, Solomos T (1998) Chlorophyllase activities and chlorophyll degradation during leaf senescence in non-yellowing mutant and wild type of Phaseolus vulgaris L. J Exp Botany 49:503–510
Timko MP (1998) Pigment biosynthesis: chlorophylls, heme, and carotenoids. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydomonas, vol 7. Springer, Dordrecht, pp 377–414
Wei ZG, Hong FS, Zhao GW (2000) Determination of double decker sandwich structure of praseodymium–chlorophyll a molecule. Chem J Chin Univ 21(3):331–334
Wei ZG, Hong FS, Tao Y, Zhao GW (2000) Determination of double decker sandwich structured La-substituted chlorophyll a by EXAFS. Acta Chimi Sin 58(5):559–562
Hong FS, Wei ZG, Zhao GW, Tao Y (2001) Determination of coordination structure metal-substituted by spectroscopy. Prog Biochem Biophys 28(3):381–386
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This work was supported by the National Natural Science Foundation of China (30800068).
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Min Zhou, Xiaolan Gong and Wang Ying contributed equally to this work.
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Zhou, M., Gong, X., Ying, W. et al. Cerium Relieves the Inhibition of Chlorophyll Biosynthesis of Maize Caused by Magnesium Deficiency. Biol Trace Elem Res 143, 468–477 (2011). https://doi.org/10.1007/s12011-010-8830-y
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DOI: https://doi.org/10.1007/s12011-010-8830-y