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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Manganese toxicity in two varieties of Douglas fir (Pseudotsuga menziesii var. viridis and glauca) seedlings as affected by phosphorus supply

Tanja Dučić A and Andrea Polle A B
+ Author Affiliations
- Author Affiliations

A Institut für Forstbotanik, Büsgenweg 2, Georg-August Universität, 37077 Göttingen, Germany.

B Corresponding author. Email: apolle@gwdg.de

Functional Plant Biology 34(1) 31-40 https://doi.org/10.1071/FP06157
Submitted: 26 June 2006  Accepted: 24 October 2006   Published: 19 January 2006

Abstract

Manganese (Mn) is an essential micronutrient in all organisms but may become toxic when present in excess. To investigate whether interior and coastal varieties of Douglas fir [Pseudotsuga menziesii (Mirbel) Franco, var. glauca (DFG) and var. viridis (DFV)] differed in Mn tolerance, seedlings were exposed to excess Mn in hydroponic solutions. Root growth, biomass production, Mn concentrations in different tissues and Mn subcellular localisation were determined. Both varieties showed similar whole-plant Mn accumulation and biomass reduction in response to increases in Mn in the nutrient solution. Since excess Mn inhibited root elongation growth more strongly in DFG than in DFV, biomass allocation in DFV was shifted towards a relative increase in root biomass and a relative decrease in DFG. X-ray microanalysis showed that Mn enrichment in cell walls and vacuoles of DFV root cortex and epidermis cells was higher than in DFG. In roots, precipitates were observed in which Mn concentrations correlated with phosphorus (P) and to a minor extent with calcium. We suggest that the higher persistence of root growth under Mn stress in DFV was caused by greater entrapment in the vacuole and in the apoplast and by more efficient Mn detoxification in insoluble complexes with P than in DFG. To investigate whether P supply affected Mn uptake and toxicity, Douglas fir seedlings were exposed to excess Mn under P deficiency. In P-limited seedlings of both varieties, roots growth was less sensitive to excess Mn than under sufficient P-supply, although in planta Mn concentrations were not diminished. In DFG, which maintained P homeostasis under limited P supply, the negative effect of Mn stress was partially reversed, showing that Mn susceptibility is affected by P metabolism.

Additional keywords: conifer, forest decline, neophytes, nutrition, phosphorus deficiency, stress.


Acknowledgements

This work was funded by the German Science Foundation (Po362/14). We are grateful to T Riemekasten for excellent technical assistance. We thank Dr E Fritz for introduction to energy dispersive X-ray transmission electron microscopy.


References


Baronius K, Fiedler HJ (1996) Nutrition status of Douglas fir (Pseudotsuga menziesii [Mirb] Franco) from Danish and German sites in comparison with the area of origin. Forstwissenschaftliches Centralblatt 115, 10–16. open url image1

Clark RB (1982) Nutrient solution growth of sorghum and corn in mineral-nutrition studies. Journal of Plant Nutrition 5, 1039–1057. open url image1

Drew MC, Saker LR (1984) Uptake and long distance transport of phosphate, potassium and chloride in relation to internal ion concentrations in barley: evidence of non-allosteric regulation. Planta 160, 500–507.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dučić T, Polle A (2005) Manganese and copper toxicity and detoxification in plants. Brazilian Journal of Plant Physiology 172, 115–122. open url image1

Dučić T, Leinemann L, Finkeldey R, Polle A (2006) Uptake and translocation of manganese in seedlings of two varieties of Douglas fir (Pseudotsuga menziesii var. viridis and glauca). New Phytologist 170, 11–20.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Farcasanu IC, Hirata D, Tsuchiya E, Nishiyama F, Miyakawa T (1995) Protein phosphatase 2B of Saccharomyces cerevisiae is required for tolerance to manganese, in blocking the entry of ions into the cells. European Journal of Biochemistry 232, 712–717.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fecht-Christoffers M, Braun HP, Lemaitre-Guillier C, VanDorsselaer A, Horst WJ (2003) Effect of manganese toxicity on the proteome of the leaf apoplast in cowpea. Plant Physiology 133, 1935–1946.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Feldman C (1974) Perchloric acid procedure for wet-ashing organics for the determination of mercury and other metals. Analytical Chemistry 46, 1606–1609.
Crossref | GoogleScholarGoogle Scholar | open url image1

Foy CD (1984) Physiological effects of hydrogen, aluminum, and manganese toxicities in acid soils. In ‘Soil acidity and liming’. 2nd edn. (Ed. F Adams) pp. 57–97. (American Society of Agronomy: Madison)

Foy CD , Scott BJ , Fisher JA (1988) Genetic differences in plant tolerance to manganese toxicity. In ‘Manganese in soils and plants’. (Eds RD Graham, RJ Hannam, NC Uren) pp. 293–307. (Kluwer Academic Publishers: Dordrecht)

Fritz E (1989) X-ray-microanalysis of diffusible elements in plant-cells after freeze-drying, pressure-infiltration with ether and embedding in plastic. Scanning Microscopy 3, 517–526. open url image1

Fritz E, Jentschke G (1994) Agar standards for quantitative X-ray-microanalysis of resin-embedded plant-tissues. Journal of Microscopy 174, 47–50. open url image1

Furihata T, Suzuki M, Sakurai H (1992) Kinetic characterization of two phosphate uptake systems with different affinities in suspension-cultured Catharanthus roseus protoplasts. Plant & Cell Physiology 33, 1151–1157. open url image1

Gonzalez A, Lynch J (1999) Tolerance of tropical common bean genotypes to manganese toxicity: performance under different growing conditions. Journal of Plant Nutrition 22, 511–525. open url image1

Gonzalez A, Steffen KL, Lynch JP (1998) Light and excess manganese. Implications for oxidative stress in common bean. Plant Physiology 118, 493–504.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Graham RD (1988) Genotypic differences in tolerance to manganese deficiency. In ‘Manganese in soils and plants’. (Eds RD Graham, RJ Hannam, NC Uren) pp. 261–276. (Kluwer Academic Publishers: Dordrecht)

Heinrichs H, Brumsack HJ, Loftfield N, König N (1986) Verbessertes Druckaufschlussystem für biologische und anorganische Materialien. Zeitschrift für Pflanzenernährung und Bodenkunde 149, 350–353. open url image1

Horiguchi T (1987) Mechanism of manganese toxicity and tolerance of plants. 2. Deposition of oxidized manganese in plant-tissues. Soil Science and Plant Nutrition 33, 595–606. open url image1

Horst WJ (1983) Factors responsible for genotypic manganese tolerance in cowpea (Vigna unguiculata). Plant and Soil 72, 213–218.
Crossref | GoogleScholarGoogle Scholar | open url image1

Horst WJ (1988) The physiology of manganese toxicity. In ‘Manganese in soils and plants’. (Eds RD Graham, RJ Hannam, NC Uren) pp. 175–188. (Kluwer Academic Publishers: Dordrecht)

Horst WJ, Marschner H (1978) Symptoms of manganese toxicity in beans (Phaseolus vulgaris L.). Zeitschrift für Pflanzenernährung und Bodenkunde 141, 129–142. open url image1

Kihn JC, Masy CL, Mestdagh MM (1988) Yeast flocculation: competition between nonspecific repulsion and specific bonding in cell adhesion. Canadian Journal of Microbiology 34, 773–778.
PubMed |
open url image1

Kitao M, Lei TT, Koike T (1997) Comparison of photosynthetic responses to manganese toxicity of deciduous broad-leaved trees in northern Japan. Environmental Pollution 97, 113–118.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kitao M, Lei TT, Nakamura T, Koike T (2001) Manganese toxicity as indicated by visible foliar symptoms of Japanese white birch (Betula platyphylla var. japonica). Environmental Pollution 111, 89–94.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kuo S, Mikkelsen DS (1980) Kinetics of zinc desorption from soils. Plant and Soil 56, 355–364.
Crossref | GoogleScholarGoogle Scholar | open url image1

Le Mare PH (1977) Experiments on effects of phosphorus on the manganese nutrition of plants. II. Interactions of phosphorus, calcium and manganese in cotton grown with nutrient solutions. Plant and Soil 47, 607–620.
Crossref | GoogleScholarGoogle Scholar | open url image1

Leinemann L (1996) Genetic differentiation of damaged and healthy Douglas fir stands in Rheinland-Pfalz with respect to their origin. Silvae Genetica 45, 250–256. open url image1

Loneragan JF (1988) Distribution and movement of manganese in plants. In ‘Manganese in soils and plants’. (Eds RD Graham, RJ Hannam, NC Uren) pp. 113–124. (Kluwer Academic Publishers: Dordrecht)

Marschner H (1986) Areas where future research on uptake and translocation of iron should be focused. Journal of Plant Nutrition 9, 1071–1076. open url image1

Marschner H (1995) ‘Mineral nutrition of higher plants.’ (Academic Press: London)

McPharlin J, Bieleski R (1987) Phosphate uptake by Spirodela and Lemna during early phosphate deficiency. Australian Journal of Plant Physiology 14, 561–572. open url image1

Memon AR, Chino M, Yatazawa M (1981) Micro-distribution of aluminum and manganese in the tea leaf tissues as revealed by X-ray microanalyzer. Communications in Soil Science and Plant Analysis 12, 441–452. open url image1

Muchhal US, Raghothama KG (1999) Transcriptional regulation of plant phosphate transporters. Proceedings of the National Academy of Sciences USA 96, 5868–5872.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nogueira MA, Magalhaes GC, Cardoso EJBN (2004) Manganese toxicity in mycorrhizal and phosphorus fertilized soybean plants. Journal of Plant Nutrition 27, 141–156.
Crossref | GoogleScholarGoogle Scholar | open url image1

Palaniyandi R, Smith CB (1979) Effect of nitrogen-sources on growth-responses and magnesium and manganese leaf concentrations of snap beans. Communications in Soil Science and Plant Analysis 10, 869–881. open url image1

Pfeffer PE, Tu S-I, Gerasimowicz WV, Cavanaugh JR (1986) In vivo 31P NMR studies of corn root tissue and its uptake of toxic metals. Plant Physiology 80, 77–84.
PubMed |
open url image1

Quiquampoix H, Loughman BC, Ratcliffe RG (1993) A 31P-NMR study of the uptake and compartmentation of manganese by maize roots. Journal of Experimental Botany 44, 1819–1827.
Crossref |
open url image1

Raghothama KG (1999) Phosphate acquisition. Annual Review of Plant Physiology and Plant Molecular Biology 50, 665–693.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Roby C, Bligny R, Douce R, Tu SI, Pfeffer PE (1988) Facilitated transport of Mn2+ in sycamore (Acer pseudoplatanus) cells and excised maize root tips. A comparative 31P NMR study in vivo. The Biochemical Journal 252, 401–410.
PubMed |
open url image1

Rout GR, Samantaray S, Das P (2001) Studies on differential manganese tolerance of mung bean and rice genotypes in hydroponic culture. Agronomie 21, 725–733.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sarkar D, Pandey SK, Sud KC, Chanemougasoundharam A (2004) In vitro characterization of manganese toxicity in relation to phosphorus nutrition in potato (Solanum tuberosum L.). Plant Science 167, 977–986.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schöne D (1991) Site and acid rain induced nutritional disorders of Douglas fir in southwestern Germany. Allgemeine Forst und Jagdzeitung 163, 53–59. open url image1

Schöne D (1992) Hypothesis and observations on manganese toxicity and trace-element nutrition of Douglas fir in southwestern Germany. Allgemeine Forst und Jagdzeitung 163, 88–93. open url image1

Shimogawara K, Usuda H (1995) Uptake of inorganic phosphate by suspension cultured tobacco cells: kinetics and regulation by Pi starvation. Plant & Cell Physiology 36, 341–351. open url image1

St Clair SB, Lynch JP (2004) Photosynthetic and antioxidant enzyme responses of sugar maple and red maple seedlings to excess manganese in contrasting light environments. Functional Plant Biology 31, 1005–1014.
Crossref | GoogleScholarGoogle Scholar | open url image1

St Clair SB, Lynch JP (2005) Element accumulation patterns of deciduous and evergreen tree seedlings on acid soils: implications for sensitivity to manganese toxicity. Tree Physiology 25, 85–92.
PubMed |
open url image1

Wissemeier AH, Horst WJ (1992) Effect of light intensity on manganese toxicity symptoms and callose formation in cowpea (Vigna unguiculata (L.) Walp.). Plant and Soil 143, 299–309.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zasoski RJ, Porada HJ, Ryan PJ, Greenleaf-Jenkins J, Gessel SP (1990) Observations of copper, zinc, iron and manganese status in western Washington forests. Forest Ecology and Management 37, 7–25.
Crossref | GoogleScholarGoogle Scholar | open url image1









Appendix 1


Table A1.  Nutrient concentrations (mg g–1 DW) in the needles, stems and roots of Douglas fir (Pseudotsuga menziesii) variety viridis (DFV) and variety glauca (DFG) after exposure to different Mn concentrations
Data indicate means (±s.d.). P-values indicate the results for main effects and interactions obtained by multifactorial analysis of variance
A1