Effects of Succinate on Manganese Toxicity in Pea Plants

ABSTRACT Pea (Pisum sativum cv. Citrine) plants were grown in nutrient solution containing various manganese (Mn) concentrations in the presence or absence of succinate to evaluate the potential role of succinate in the plant tolerance to Mn excess. Supplying pea plants with excess Mn led to a reduction in the relative growth rate (RGR), chlorophyll a and b content, photosynthetic O2 evolution activity, and photosystem II (PSII) activity, as measured in the light-adapted state (φPSII) in comparison to the control. The primary photochemical efficiency of PSII, estimated by the Fv/Fm ratio, was less affected by increasing Mn concentration. Chloroplasts from Mn-treated leaves exhibited significant changes in their ultrastructure, depending on the strength of Mn toxicity. The concentration of Mn in roots, stem, and leaves increased with the increase of Mn in the nutrient solution. Addition of succinate before and after Mn treatment did not reduce the inhibitory effect of Mn on the plant growth, chlorophyll fluorescence parameters, photosynthetic O2 evolution activity, and chloroplast structure of the pea plants. It was found that supply of exogenous succinate at a high Mn concentration (over 1500 μM) in the nutrient solution led to an increase of Mn uptake in the roots accompanied by a decrease in a Mn translocation to the leaves and stems compared to Mn-treated pea-plants. However, differences in the toxicity effect of Mn in both Mn and Mn/Succinate-treated pea plants were not detected. Thus, such changes in Mn distribution within the Mn/succinate-treated plant did not confer tolerance of Mn excess to pea plants. These results suggest that succinate probably has an affinity for Mn and may function as a “terminal acceptor” of large amounts of Mn, decreasing Mn transport to the stem and leaves, but does not contribute to Mn tolerance.

[1]  D. R. Hoagland,et al.  The Water-Culture Method for Growing Plants Without Soil , 2018 .

[2]  F. Lidon,et al.  Rice tolerance to excess Mn: Implications in the chloroplast lamellae and synthesis of a novel Mn protein , 2000 .

[3]  K. Hirschi,et al.  Expression of arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. , 2000, Plant physiology.

[4]  F. Lidon.  Rice adaptation to excess manganese : Nutrient accumulation and implications of the quality of crops , 2000 .

[5]  D. Subrahmanyam,et al.  Influence of Manganese Toxicity on Photosynthesis in Ricebean (Vigna Umbellata) Seedlings , 2000, Photosynthetica.

[6]  R. Wise,et al.  The ultrastructure of chilling stress , 2000 .

[7]  T. Pandolfini,et al.  A physiological characterization of Mn-tolerant tobacco plants selected by in vitro culture , 2000 .

[8]  W. Horst,et al.  Physiology of manganese toxicity and tolerance in Vigna unguiculata (L.) Walp. , 1999 .

[9]  Steffen,et al.  Light and excess manganese . Implications for oxidative stress in common bean , 1998, Plant physiology.

[10]  G. Santandrea,et al.  Effects of manganese on Nicotiana species cultivated in vitro and characterization of regenerated Mn-tolerant tobacco plants , 1998 .

[11]  D. Cox,et al.  Manganese toxicity in plants , 1998 .

[12]  J. Lynch,et al.  Effects of manganese toxicity on leaf CO2 assimilation of contrasting common bean genotypes , 1997 .

[13]  T. Koike,et al.  Effects of manganese toxicity on photosynthesis of white birch (Betula platyphylla var. japonica) seedlings , 1997 .

[14]  Michael Moustakas,et al.  Physiological and Ultrastructural Effects of Cadmium on Wheat (Triticum aestivum L.) Leaves , 1997, Archives of environmental contamination and toxicology.

[15]  J. Vangronsveld,et al.  Copper toxicity in young maize (Zea mays L.) plants: effects on growth, mineral and chlorophyll contents, and enzyme activities , 1996, Plant and Soil.

[16]  B. Carver,et al.  Acid soil tolerance in wheat , 1995 .

[17]  G. Taylor,et al.  Effects of Excess Manganese on Production of Organic Acids in Mn-Tolerant and Mn-Sensitive Cultivars of Triticum aestivum L. (Wheat) , 1994 .

[18]  G. Taylor,et al.  The effects of excess manganese on photosynthetic rate and concentration of chlorophyll in Triticum aestivum grown in solution culture , 1992 .

[19]  Esa Tyystjärvi,et al.  A microcomputer program and fast analog to digital converter card for the analysis of fluorescence induction transients , 1990, Photosynthesis Research.

[20]  R. Nable,et al.  Early Inhibition of Photosynthesis during Development of Mn Toxicity in Tobacco. , 1988, Plant physiology.

[21]  T. Horiguchi.  Mechanism of manganese toxicity and tolerance of plants. , 1987 .

[22]  W. Horst,et al.  Callose deposition in leaves of cowpea (Vigna unguiculata [L.] Walp.) as a sensitive response to high Mn supply , 1987, Plant and Soil.

[23]  K. Aoba.  Excess Manganese Disorder in Fruit Trees , 1986 .

[24]  A. Memon,et al.  Nature of manganese complexes in manganese accumulator plant. Acanthopanax sciadophylloides , 1984 .

[25]  R. Wise,et al.  A comparative study of low-temperature-induced ultrastructural alterations of three species with differing chilling sensitivities , 1983 .

[26]  Werner Mathys,et al.  The Role of Malate, Oxalate, and Mustard Oil Glucosides in the Evolution of Zinc‐Resistance in Herbage Plants , 1977 .

[27]  P. Morgan,et al.  Manipulation of IAA‐Oxidase Activity and Auxin‐Deficiency Symptoms in Intact Cotton Plants with Manganese Nutrition , 1976 .

[28]  J. L. Fowler,et al.  The relationship of the peroxidative indoleacetic Acid oxidase system to in vivo ethylene synthesis in cotton. , 1972, Plant physiology.

[29]  E. Reynolds.  THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY , 1963, The Journal of cell biology.

[30]  G. Mackinney,et al.  ABSORPTION OF LIGHT BY CHLOROPHYLL SOLUTIONS , 1941 .

[31]  W. Bilger,et al.  Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer , 2004, Photosynthesis Research.

[32]  F. Lidon.  Tolerance of rice to excess manganese in the early stages of vegetative growth. Characterisation of manganese accumulation , 2001 .

[33]  J. Hagemeyer.  Ecophysiology of Plant Growth Under Heavy Metal Stress , 1999 .

[34]  E. Olivares,et al.  Manganese tolerance in Clusia multiflora (H.B.K.) , 1998 .

[35]  W. Van Camp,et al.  Superoxide Dismutase in Plants , 1994 .

[36]  G. Krause,et al.  The Photosynthetic Apparatus and Chlorophyll Fluorescence. An Introduction , 1988 .

[37]  R. Chaney,et al.  The Physiology of Metal Toxicity in Plants , 1978 .

[38]  W. L. Butler.  Chlorophyll Fluorescence: A Probe for Electron Transfer and Energy Transfer , 1977 .

[39]  W. Loomis.  Overcoming problems of phenolics and quinones in the isolation of plant enzymes and organelles. , 1974, Methods in enzymology.

[40]  D. Arnon.  COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. , 1949, Plant physiology.