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Contrasting Performance and Different Tolerance of Chestnut Rose and Grape to Excess Manganese

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Abstract

Grape (cultivar Jinshou) and chestnut rose (cultivar Gui 4) were exposed to excess manganese (Mn) treatments to characterize the physiological basis for Mn tolerance in woody plants. Chestnut rose exhibited a high sensitivity to this environmental constraint whereas grape appeared rather tolerant to Mn excess. Stomatal density and closure rate were affected by excess Mn in chestnut rose and brittleness of the leaf vein was reported as a novel Mn toxicity symptom in this species. Linear reductions in biomass accumulation and photosynthetic pigment concentrations with increasing Mn level were observed in chestnut rose but not in grape, except under the extremely high Mn concentration (118 mM). Our results showed that the contrasting performances between the two species were related to the differences in ion transfer and homeostasis. Mn was readily allocated to the photosynthetic organ in chestnut rose but was mainly restricted to the roots in grape. Excess Mn caused iron (Fe) and nitrogen (N) deficiencies in chestnut rose but not in grape. The synthesis of antioxidant phenylpropanoid compounds and chelating phytochelatins were activated in Mn-treated grape but strongly repressed in chestnut rose. The importance of these parameters in the overall strategy of Mn tolerance in grape is discussed.

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References

  • Beer J, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    Google Scholar 

  • Blum R, Beck A, Korte A, Stengel A, Letzel T, Lendzian K, Grill E (2007) Function of phytochelatin synthase in catabolism of glutathione-conjugates. Plant J 49:740–749

    Article  PubMed  CAS  Google Scholar 

  • Bot JL, Goss MJ, Carvalho MJGPR, Van Beusichem ML, Kirkby EA (1990) The significance of the magnesium to manganese ratio in plant tissues for growth and alleviation of manganese toxicity in tomato (Lycopersicon esculentum) and wheat (Triticum aestivum) plants. Plant Soil 124:205–210

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Cailliatte R, Schikora A, Briat JF, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22(3):904–917

    Article  PubMed  CAS  Google Scholar 

  • Chaney RL (1993) Zinc phytotoxicity. In: Robson AD (ed) Zinc in Soils and Plants. Kluwer Academic, London

    Google Scholar 

  • Clarkson DT (1988) The uptake and translocation of manganese by plant roots. In: Graham RD, Hannam RJ, Uren NC (eds) Manganese in Soils and Plants. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Cobbett CS, May MJ, Howden R, Rolls B (1998) The glutathione-deficient, cadmium-sensitive mutant, cad2–1, of Arabidopsis thaliana is deficient in gamma-glutamylcysteine synthetase. Plant J 16:73–78

    Article  PubMed  CAS  Google Scholar 

  • Doncheva S, Poschenrieder C, Stoyanova Z, Georgieva K, Velichkova M, Barceló J (2009) Silicon amelioration of manganese toxicity in Mn-sensitive and Mn-tolerant maize varieties. Environ Exp Bot 65:189–197

    Article  CAS  Google Scholar 

  • Dučić T, Leinemann L, Finkeldey R, Polle A (2006) Uptake and translocation of manganese in cuttings of two varieties of Douglas fir (Pseudotsuga menziesii var. viridis and glauca). New Phytol 170:11–20

    Article  PubMed  Google Scholar 

  • El-Jaoual T, Cox DA (1998) Manganese toxicity in plants. J Plant Nutr 21:353–386

    Article  CAS  Google Scholar 

  • Ernst W, Krauss GJ, Verkleij J, Wesenberg D (2008) Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143

    PubMed  CAS  Google Scholar 

  • Foy CD (1984) Physiological effects of hydrogen, aluminum, and manganese toxicities in acid soil. In: Adams F (ed) Soil acidity and liming, 2nd edn. ASA, CSSA, and SSSA Book Publishing, Madison

    Google Scholar 

  • Ghanati F, Ishka MR (2006) Improvement of antioxidant system and decrease of lignin by nickel treatment in tea plant. J Plant Nutr 29:1649–1661

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutase in higher plants. Plant Physiol 59:309–314

    Article  PubMed  CAS  Google Scholar 

  • Goss MJ, Carvalho MJGPR (1992) Manganese toxicity: The significance of magnesium for the sensitivity of wheat plants. Plant Soil 139:91–98

    Article  CAS  Google Scholar 

  • Grill E, Winnacker EL, Zenk MH (1987) Phytochelatins, a class of heavy metal-binding peptides from plants, are functionally analogous to metallothioneins. Proc Natl Acad Sci USA 84:439–443

    Article  PubMed  CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  PubMed  CAS  Google Scholar 

  • Ishimaru Y, Masuda H, Bashir K, Inoue H, Tsukamoto T, Takahashi M, Nakanishi H, Aoki N, Hirose T, Ohsugi R, Nishizawa NK (2010) Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J 62:379–390

    Article  PubMed  CAS  Google Scholar 

  • Kabata-Pendias A, Pendias H (2001) Trace Elements in Soils and Plants, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

  • Lei Y, Chen K, Tian X, Korpelainen H, Li C (2007) Effect of Mn toxicity on morphological and physiological changes in two Populus cathayana populations originating from different habitats. Trees 21:569–580

    Article  CAS  Google Scholar 

  • Lidon FC, Teixeira MG (2000) Rice tolerance to excess Mn: implications in the chloroplast lamellae and synthesis of a novel Mn protein. Plant Physiol Biochem 38:969–978

    Article  CAS  Google Scholar 

  • Lidon FC, Ramalho JC, Graça MG (2004) Manganese accumulation in rice: implications for photosynthetic functioning. J Plant Physiol 161:1235–1244

    Article  PubMed  CAS  Google Scholar 

  • MacFarlane GR, Burchett MD (2001) Photosynthetic pigments and peroxidase activity as indicators of heavy metal stress in the grey mangrove. Avicennia marina (Forsk.) Vierh Mar Poll Bull 42:233–240

    Article  CAS  Google Scholar 

  • May MJ, Vernoux T, Sánchez-Fernández R, Van Montagu M, Inzé D (1998) Evidence for posttranscriptional activation of g-glutamylcysteine synthetase during plant stress response. Proc Natl Acad Sci USA 95:12049–12054

    Article  PubMed  CAS  Google Scholar 

  • Moran R, Porath D (1980) Chlorophyll determination in intact tissues using N, N-dimethylformamide. Plant Physiol 65:478–479

    Article  PubMed  CAS  Google Scholar 

  • Moria S, Uraguchi S, Ishikawa S, Arao T (2009) Xylem loading process is a critical factor in determining Cd accumulation in the shoots of Solanum melongena and Solanum torvum. Environ Exp Bot 67:127–132

    Article  Google Scholar 

  • Mou D, Yao Y, Yang Y, Zhang Y, Tian C, Achal V (2011) Plant high tolerance to excess manganese related with root growth, manganese distribution and antioxidative enzyme activity in three grape cultivars. Ecotoxicol Environ Saf 74:4776–4786

    Article  Google Scholar 

  • Nickel RS, Cunningham BA (1969) Improved peroxidase assay method using leuco 2,3,6-trichloroindophenol and application to comparative measurements of peroxidase catalysis. Anal Biochem 27:292–299

    Article  PubMed  CAS  Google Scholar 

  • Padmavathiamma P, Li L (2009) Phytostabilisation - A sustainable remediation technique for zinc in soils. Water Air Soil Pollut 9:253–260

    Article  CAS  Google Scholar 

  • Page AL (1982) Methods of soil analysis (Part 2), 2nd edn. American Society of Agronomy, Madison

    Google Scholar 

  • Paschke MW, Valdecantos A, Redente EF (2005) Manganese toxicity thresholds for restoration grass species. Environ Pollut 135:313–322

    Article  PubMed  CAS  Google Scholar 

  • Pittman JK (2005) Managing the manganese: molecular mechanisms of manganese transport and homeostasis. New Phytol 167:733–742

    Article  PubMed  CAS  Google Scholar 

  • Polle TDA (2005) Transport and detoxification of manganese and copper in plants. Braz J Plant Physiol 17:103–112

    Article  Google Scholar 

  • Rauser WE (1995) Phytochelatins and related peptides (structure, biosynthesis, and function). Plant Physiol 109:141–1149

    Google Scholar 

  • Reeves RD (2006) Hyperaccumulation of trace elements by plants. In: Morel JL, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils. Springer, Berlin

    Google Scholar 

  • Rengel Z (2004) Heavy metals as essential nutrients. In: Prasad MN (ed) Heavy Metal Stress in Plants: From Biomolecules to Ecosystems, 2nd edn. Springer-Verlag, Berlin

    Google Scholar 

  • Rice-Evans CA, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2:152–159

    Article  Google Scholar 

  • Tokusoglu O, Unal MK, Yildirum Z (2003) HPLC-UV and GC-MS characterization of the flavonol aglycons quercetin, kaempferol and myricetin in tomato and tomato pastes and other tomato-based products. Acta Chromatogr 13:196–207

    CAS  Google Scholar 

  • Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2010) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688

    Article  Google Scholar 

  • Wen XP, Deng XX (2005) Micropropagation of Guinong 4 cultivar (Rosa roxburghii Tratt) and genetic stability assessment of the in vitro plants using RAPD and AFLP markers. J Hort Sci Biotech 80:54–60

    CAS  Google Scholar 

  • Yang SX, Deng H, Li MS (2008) Manganese uptake and accumulation in a woody hyperaccumulator, Schima superb. Plant Soil Environ 54:441–446

    CAS  Google Scholar 

  • Zheng Y, Dai X, Wang L, Xu W, He Z, Ma M (2008) Arsenate reduces copper phytotoxicity in gametophytes of Pteris vittata. J Plant Physiol 165:1906–1916

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the “100 Distinguished Young Scientists” Program of the Chinese Academy of Science, the National Scientific Foundation in China (No. 30800127), and the program of “Guizhou Outstanding Youth Talent in Science and Technology.”

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Correspondence to Yin An Yao.

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Yao, Y.A., Mou, D., Xu, G. et al. Contrasting Performance and Different Tolerance of Chestnut Rose and Grape to Excess Manganese. J Plant Growth Regul 31, 416–426 (2012). https://doi.org/10.1007/s00344-011-9251-7

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  • DOI: https://doi.org/10.1007/s00344-011-9251-7

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