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

Photosynthetic and antioxidant enzyme responses of sugar maple and red maple seedlings to excess manganese in contrasting light environments

Samuel B. St. Clair A and Jonathan P. Lynch A B
+ Author Affiliations
- Author Affiliations

A Intercollegiate Graduate Program in Ecological and Molecular Plant Physiology, The Pennsylvania State University, 102 Tyson Building, University Park, PA 16802, USA.

B Department of Horticulture, The Pennsylvania State University, 221 Tyson Building, University Park, PA 16802, USA. Corresponding author; email: JPL4@psu.edu

Functional Plant Biology 31(10) 1005-1014 https://doi.org/10.1071/FP04049
Submitted: 27 February 2004  Accepted: 9 August 2004   Published: 14 October 2004

Abstract

Manganese (Mn) toxicity may be a significant constraint to forest health on acidic, non-glaciated soils. We hypothesised that sugar maple (Acer saccharum Marsh.) and red maple (Acer rubrum L.) seedlings differ in their tolerance to excess Mn, and that photosynthetic sensitivity to excess Mn is exacerbated at higher light intensities through photo-oxidative stress. To test these hypotheses, we assessed photosynthesis and antioxidant enzyme responses of sugar maple and red maple seedlings at variable Mn and light levels in a greenhouse study. In both species, high Mn treatments impaired photosynthetic function, particularly in high light conditions. Responses to Mn and light depended on the developmental stage of the leaves. All sugar maple leaves were sensitive to Mn toxicity except shaded young leaves. For red maple, only mature leaves exposed to high light were prone to Mn toxicity. Antioxidant enzyme and ФPSII / ФCO2 data suggested that photo-oxidative stress did not explain the observed photosynthetic responses to treatment variables. Our results indicate that in natural forest environments, sugar maple and red maple foliage exposed to high light intensity (outer canopy, canopy gaps) may be more prone to Mn toxicity.

Keywords: chlorophyll, metals, nutrition, photo-oxidation, photosynthesis, stress.


Acknowledgments

This research was supported by USDA (NRI) grant #2002-35100-12055 to JP Lynch and JC Carlson.


References


Abrams MD (1998) The red maple paradox. Bioscience 48, 355–364. open url image1

Bernier B, Brazeau M (1988a) Foliar nutrient status in relation to sugar maple dieback and decline in the Quebec Appalachians. Canadian Journal of Forest Research 18, 754–761. open url image1

Bernier B, Brazeau M (1988b) Nutrient deficiency symptoms associated with sugar maple dieback and decline in the Quebec Appalachians. Canadian Journal of Forest Research 18, 762–767. open url image1

Bueno P, Piqueras A (2002) Effect of transition metals on stress, lipid peroxidation and antioxidant enzyme activities in tobacco cell cultures. Plant Growth Regulation 36, 161–167.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 Physiology 98, 1222–1227. open url image1

Christeller T, Laing W (1979) Effects of manganese ions and magnesium ions on the activity of soya-bean ribulose bisphosphate carboxylase / oxygenase. The Biochemical Journal 183, 747–750.
PubMed |
open url image1

Cronan CS, Grigal DF (1995) Use of calcium / aluminum ratios as indicators of stress in forest ecosystems. Journal of Environmental Quality 24, 209–226. open url image1

Driscoll CT, Lawrence GB, Bulger AJ, Butler TJ, Cronan CS, Eagar C, Lambert KF, Likens GE, Stoddard JL, Weathers KC (2001) Acidic deposition in the northeastern United States: sources and inputs, ecosystem effects, and management strategies. Bioscience 51, 180–198. open url image1

Drohan PJ, Stout SL, Petersen GW (2002) Sugar maple (Acer saccharum Marsh.) decline during 1979–1989 in northern Pennsylvania. Forest Ecology and Management 170, 1–17.
Crossref | GoogleScholarGoogle Scholar | open url image1

Duchesne L, Ouimet R, Houle D (2002) Basal area growth of sugar maple in relation to acid deposition, stand health, and soil nutrients. Journal of Environmental Quality 31, 1676–1683.
PubMed |
open url image1

El-Jaoual T, Cox DA (1998) Manganese toxicity in plants. Journal of Plant Nutrition 21, 353–386. open url image1

Foy C, Scott B, Fisher J (1988) Genetic differences in plant tolerance to manganese toxicity. ‘Manganese in soils and plants’. (Eds R Graham, J Hannam, N Uren) pp. 293–307. (Kluwer Academic Publishers: Dordrecht)

Fryer MJ, Andrews JR, Oxborough K, Blowers DA, Baker NR (1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiology 116, 571–580.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gawel JE, Ahner BA, Friedland JA, Morel FMM (1996) Role for heavy metals in forest decline as indicated by phytochelatin measurements. Nature 381, 64–65.
Crossref | GoogleScholarGoogle Scholar | open url image1

Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92. open url image1

Gonzalez A, Lynch JP (1997) Effects of manganese toxicity on leaf CO2 assimilation of contrasting common bean genotypes. Physiologia Plantarum 101, 872–880.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gonzalez A, Lynch JP (1999) Subcellular and tissue Mn compartmentation in bean leaves under Mn toxicity stress. Australian Journal of Plant Physiology 26, 811–822. 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

Gumpertz ML, Brownie C (1993) Repeated measures in randomized block and split-plot experiments. Canadian Journal of Forest Research 23, 625–639. open url image1

Horsley SB, Long RP, Bailey SW, Hallett RA, Hall TJ (2000) Factors associated with the decline disease of sugar maple on the Allegheny Plateau. Canadian Journal of Forest Research 30, 1365–1378.
Crossref | GoogleScholarGoogle Scholar | open url image1

Houtz R, Nable R, Cheniae G (1988) Evidence for effects on the in vivo activity of ribulose-bisphosphate carboxylase / oxygenase during development of Mn toxicity in tobacco. Plant Physiology 86, 1143–1149. open url image1

Huttl, RF ,  and  Schaaf, W (1997). ‘Magnesium deficiency in forest ecosystems.’ (Kluwer Academic Publishers: Dordrecht)

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, Koike T (1998) Application of chlorophyll fluorescence to evaluate Mn tolerance of deciduous broad-leaved tree seedlings native to northern Japan. Tree Physiology 18, 135–140.
PubMed |
open url image1

Kobe RK, Likens GE, Eagar C (2002) Tree seedling growth and mortality responses to manipulations of calcium and aluminum in a northern hardwood forest. Canadian Journal of Forest Research 32, 954–966.
Crossref | GoogleScholarGoogle Scholar | open url image1

Krupa A, Baszynski T (1995) Some aspects of heavy metals toxicity towards photosynthetic apparatus-direct and indirect effects on light and dark reactions. Acta Physiologiae Plantarum 17, 177–190. open url image1

Krupa Z, Moniak M (1998) The stage of leaf maturity implicates the response of the photosynthetic apparatus to cadmium toxicity. Plant Science 138, 149–156.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lidon FC, Teixeira MG (2000) Oxy radicals production and control in the chloroplast of Mn-treated rice. Plant Science 152, 7–15.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lucas RE, Davis JF (1961) Relationship between pH values of organic soils and availabilities of 12 plant nutrients. Soil Science 92, 177–182. open url image1

Maksymiec W, Baszynski T (1996) Different susceptibility of runner bean plants to excess copper as a function of growth stages of primary leaves. Journal of Plant Physiology 149, 217–221. open url image1

Marschner H, Cakmak I (1989) High light intensity enhances chlorosis and necrosis in leaves of zinc-, potassium- and magnesium-deficient bean (Phaseolus vulgaris) plants. Journal of Plant Physiology 134, 308–315. open url image1

Massacci A, Iannelli MA, Pietrini F, Loreto F (1995) The effect of growth at low-temperature on photosynthetic characteristics and mechanisms of photoprotection of maize leaves. Journal of Experimental Botany 46, 119–127. open url image1

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence — a practical guide. Journal of Experimental Botany 51, 659–668.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McCain DC, Markley JL (1989) More manganese accumulates in maple sun leaves than in shade leaves. Plant Physiology 90, 1417–1421. open url image1

McQuattie CJ, Schier GA (2000) Response of sugar maple (Acer saccharum) seedlings to manganese. Canadian Journal of Forest Research 30, 456–467.
Crossref | GoogleScholarGoogle Scholar | open url image1

McWilliams WH, White R, Arner SL, Nowak CA, Stout SL (1996) Characteristics of declining forest stands on the Allegheny National Forest. Research Note NE-360, 1–9. USDA Forest Service.

Nable RO, Houtz RL, Cheniae GM (1988) Early inhibition of photosynthesis during development of Mn toxicity in tobacco. Plant Physiology 86, 1136–1142. open url image1

Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867–880. open url image1

Pell EJ, Sinn JP, Brendley BW, Samuelson L, Vinten-Johansen C, Tien M, Skillman J (1999) Differential response of four tree species to ozone-induced acceleration of foliar senescence. Plant, Cell and Environment 22, 779–790.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sharpe, WE ,  and  Drohan, JR (1999). ‘The effects of acidic deposition on Pennsylvania’s forests.’ (Environmental Resources Research Institute: University Park)

Smirnoff N (1993) The role of active oxygen in the response of plants to water-deficit and desiccation. Tansley Review 52. New Phytologist 125, 27–58. open url image1

Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissues homogenates using 5,5′-dithiobis (2-nitrobenzoic acid). Analytical Biochemistry 175, 408–413.
PubMed |
open url image1

St. Clair SB (2004) ‘Factors and mechanisms underlying sugar maple sensitivity to edaphic stresses on Pennsylvania’s Allegheny Plateau.’ PhD Thesis. (Pennsylvania State University: PA.)

Tomlinson GH (2003) Acidic deposition, nutrient leaching and forest growth. Biogeochemistry 65, 51–81.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tomlinson, GH ,  and  Tomlinson, FL (1990). ‘Effects of acid deposition on the forests of Europe and North America.’ (CRC Press: Boca Raton)

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387. open url image1

Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313. open url image1

Wildner GF, Henkel J (1978) Differential reactivation of ribulose 1,5-bisphosphate oxygenase with low carboxylase activity by Mn2+. FEBS Letters 91, 99–103.
Crossref | GoogleScholarGoogle Scholar | open url image1