Comparison of photosynthetic responses to manganese toxicity of deciduous broad-leaved trees in northern Japan

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S0269-7491

Environmental Pollution, Vol. 97, No. 1-2, pp. 113-118, 1997 © 1997 Elsevier Science Ltd All rights reserved. Printed in Great Britain (97)00064-X 0269-7491/97517.00+0.00

ELSEVIER

COMPARISON OF PHOTOSYNTHETIC RESPONSES TO M A N G A N E S E TOXICITY OF D E C I D U O U S BROAD-LEAVED TREES IN N O R T H E R N JAPAN M . K i t a o , * T. T. Lei* a n d T. K o i k e ~ Forestry and Forest Products Research Institute, Hokkaido Research Center, Sapporo 062, Japan

(Received 7 October 1996; accepted 28 April 1997)

and Al (Fernandez, 1989). Beech leaves were reported to have high Mn concentrations in southern Sweden where soils were affected by acid precipitation (Balsberg Pfihlsson, 1989). However, it is difficult to determine whether a given Mn concentration in a leaf is toxic or not because plant species show different levels of tolerance and sensitivity for excess Mn (for review see Foy et ak, 1978). Therefore, it is necessary to first establish what concentration of Mn in the leaves of different tree species constitutes toxicity. In northern Japan, early successional species such as birch and willow were observed to grow in the sparsely vegetated acid sulfate soils with pH levels below 5 (Sanada, 1986). This suggests an adaptive capacity of these early successional species in acid soils to maintain carbon uptake even when leaves contain high levels of Mn. In an early study, we found a higher tolerance to Mn toxicity in white birch (Betula platyphylla var. japonica), an early successional species (Kitao, 1996; Kitao et al., 1997) than herbaceous species such as tobacco and wheat, based on net photosynthetic rate (Ohki, 1985; Nable et al., 1988). Manganese toxicity is known to increase the activity of enzymes such as polyphenol oxidase, peroxidase and indoleacetic acid (IAA) oxidase, to interact with other essential nutrients and to cause a decrease in yield (see review in Horst, 1988). While the mechanism linking Mn toxicity to assimilation is still not well understood, photosynthesis is among the most sensitive plant processes to Mn toxicity since the decline of photosynthesis precedes chlorophyll degradation and visible foliar symptoms (Nable et al., 1988). In the northern broad-leaved forests of Japan, species of different successional traits exhibit different photosynthetic capacities closely related to their leaf structures (Koike, 1988). Compared with late successional species, early successional species have higher mesophyll surface area per unit leaf area (Ames A-l), (Koike, 1988), thus increasing the mesophyll conductance for CO2 diffusion (Nobel, 1977). They also have higher photosynthetic capacity under high light. Late successional species have lower Ames A -1 and higher photosynthetic rates under low light, and mid-successional species show intermediate properties.

Abstract The effects of manganese (Mn) toxicity on photosynthesis of four tree species in northern Japan representing different successional traits were examined. The four species are: Betula ermanii (Be) and Alnus hirsuta (Ah) representing two early successional species, Ulmus davidiana var. japonica (Ud) as the mid-successional species, and Acer mono (Am) as the late successional species. Seedlings were grown hydroponically in a solution containing nutrients and Mn of four concentrations (1, 10, 50, lOOmglitre -1) for 50 days. Gas exchange measurements indicate that in all species, Mn accumulation in leaves resulted in the decline of light-saturated net photosynthetic rate at ambient C02 pressure (35 Pa, Pnamb) and at saturating ( 5 % ) C02 pressure (Pnsat), and of carboxylation efficiency but has little effect on the maximum efficiency of photochemistry. Sensitivity to elevated levels of Mn differed among species where the decline of Pnamb was much more modest in the two early successional species of Be and Ah than the mid- and late successional spec&s of Ud and Am. The same trends were observed in both Pnsat and carboxylation efficiency. Based on these results, we suggest that early successional species (Betula ermanii and Alnus hirsuta) have greater tolerance for excess Mn in leaves than mid- and late successional species. © 1997 Elsevier Science Ltd

Keywords: Carboxylation efficiency, Mn tolerance, net photosynthesis, quantum yield, RuBP regeneration. INTRODUCTION

Manganese toxicity constitutes a major adverse effect on plants grown in acid soils (Sumner et al., 1991). Soil acidification is considered one of the main causes of forest decline due to 'acid rain' (Haines and Carlson, 1989) as it increases leaching of cations such as Mg and Ca, and enhances solubility of toxic metals such as Mn *To whom correspondence should be addressed. Fax: + 81 11 8514167, e-mail: [email protected] *Present address: Biology Department, Virginia Polytechnic Institute and State University, Biacksburg, VA 24061, USA. ~Present address: Forest Science Research, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183, Japan. 113

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We hypothesized that the higher tolerance to Mn toxicity of early successional species is related to their photosynthetic properties and associated leaf structures. Our aim in this study was to examine how Mn toxicity affects the photosynthesis of different successional tree species through gas exchange measurements. By comparing the response patterns of species to elevated levels of Mn, we may deduce a plausible mechanism that regulating the species-specific tolerance level to Mn toxicity.

MATERIALS AND METHODS Plant materials We examined four broad-leaved tree species. Their successional status, as described by Kikuzawa (1983) and Koike (1988), are Alnus hirsuta (Ah) and Betula ermanii (Be): early successional species, Ulmus davidiana var. japonica (Ud): mid-successional species and Acer mono (Am): late successional species. Two-years-old seedlings of Be, Ah and Ud and 3-years-old seedlings of Am from a tree nursery (Oji Forestry and Landscaping Co., Ltd., Sapporo, Japan) were used. Seedlings of these four species were cultivated hydroponically in trays with 1001itre of a well aerated nutrient solution containing 40.0 (N), 10.8 (P), 27.2 (K), 6.1 (Mg), 14.3 (Ca), and 5.0 mglitre -1 (Fe) plus micronutrients. The trays were set in a glasshouse exposed to natural daylight. The initial size of the bare root seedlings was 20-30cm in height. After an initial period of establishment for 2 weeks in the trays, four Mn concentrations were applied: 1 (control), 10, 50 and 100mglitre -1 in the form of MnCI2.2H20. The solution of nutrients and Mn in each tray was completely replaced once every 10 days. Measurement of photosynthetic gas exchange C O 2 assimilation rate was measured in two ways. First, net photosynthesis was determined on attached, fullyexpanded leaves that had developed after the start of the Mn treatment. Maximum photosynthesis was determined on a 21-28 day-old leaf on the leader shoot of each plant since these leaves have been shown to attain maximum rates based on age-dependent photosynthesis in several broad-leaved tree species (Koike, 1990). One leaf each of three to five plants per treatment was measured with an open system infrared gas analyzer (Model H3, Analytical Development Company, UK). Lightsaturated net photosynthesis at ambient CO2 of 35 Pa (Pnamb), 13Pa and 0Pa were measured at 25°C, the optimum leaf temperature for all species (Koike and Sakagami, 1985). Artificial light at 1100/~mol m -2 s -l photosynthetic photon flux density (PPFD) was provided by a cool halogen lamp (fiber optic light source, Nikon, Tokyo, Japan). Carboxylation efficiency (CE) was derived from the slope in CO2 assimilation rate versus intercellular CO2 pressures (Ci) at Ca of 13 Pa and 0Pa (von Caemmerer and Farquhar, 1981; Farquhar and Sharkey, 1982) based on an assumption of uniform response of stomata (Terashima, 1992).

Second, net photosynthesis at saturating C O 2 (5O,/o, Pnsat) was measured by oxygen evolution of leaf discs (3.14cm 2) in the gas phase with a Hansatech Oxygen Electrodes in a thermostat-controlled chamber at 25°C, (Model LD2, Hansatech Instruments Ltd., King's Lynn, Norfolk, UK). At saturating CO2, light-saturated photosynthesis is generally limited by the rate of RuBP regeneration since limitations of diffusional process and rubisco carboxylation are removed at such a high CO2 condition (von Caemmerer and Farquhar, 1981; Farquhar and Sharkey, 1982). One disk per leaf from each of three to five plants was used. A halogen lamp (Model LS2, Hansatech Instruments Ltd.) provided the light source at 900 and 50 #mol m -2 s -I PPFD through neutral density filters. Dark respiration was measured by shutting off the light source. We assumed that at a photon flux density of 50#molm-2s-% as used in the present study, is low enough to capture the initial slope of light response curve according to other studies of light-dependent photosynthesis (Osmond et aL, 1980; Linder et al., 1981; Koike, 1986). The maximum quantum yield of 02 evolution (~o), corrected for leaf absorptance, was derived from the slope of 02 evolution rate at 0 (dark respiration rate) and 50/zmolm-2s -1 PPFD. The correction of quantum yield of 02 evolution for leaf absorptance was made by estimating leaf absorptance from the relationship between leaf absorptance and SPAD values (r2> 0.87, significant at p<0.01 for each species). SPAD values which have close correlation with leaf chlorophyll content were measured using a SPAD chlorophyll meter (SPAD 502, Minolta, Osaka, Japan). Leaf reflectance (R) and transmittance (Tr) were measured at 400-700 nm using a spectroradiometer (Li-1800C; Li-Cor Inc., Lincoln, NE, USA) with an external integrating sphere (LI1800-12S, Lei et al., 1996). Total absorptance was calculated as 1 - ( R + Tr). Manganese determination in leaves Leaves used for gas exchange measurements were removed from the plants, rinsed with de-ionized water, then dried in an oven at 80°C for 3 days. Each sample was digested with a HCIO4 and HNO3 mixture. The leaf Mn concentration was then analyzed with an atomic absorption spectrophotometer (Model 180-50, Hitachi, Tokyo, Japan). Statistics All measurements of gas exchange were done once per leaf and replicated in several plants. All data points were used in the least squares linear regression among measured parameters, and carried out independently for each species.

RESULTS Visible symptoms Leaves of all tree species developed some visible symptoms in treatments greater than 1 mglitre -~ Mn. In

Mn toxicity and photosynthesis general, young leaves, especially those expanded after the Mn treatments, developed chlorosis and old leaves developed dark-brown spots and necrosis. Am which did not emerge new leaves after Mn treatments showed brown spots over the whole leaf and subsequent necrosis along the leaf edge. Older leaves of Be had brown spots in the interveinal area and leaf edge, but no spots adjacent to the veins. Ah leaves showed dark-brown spots in the interveinal area and necrosis along the leaf edge. Ud in the two highest treatments of 50 and 100mglitre-~Mn were so severely affected that no leaves were suitable for measurements. The older leaves of Ud exhibited black coloration on their veins and dark-brown spots over the leaves. Even when leaf Mn concentrations in early successional species (Be and Ah) were apparently higher than mid- and late successional species (Ud and Am) at the same Mn treatments (Fig. 1), only interveinal brown spots were seen on leaves of Be and Ah at more than 10000/zgg -1 dry wt Mn. In contrast, brown spots covering the entire leaf could occur in Ud and Am at less than 10000/zgg -~ dry wt Mn. Light-saturated net photosynthesis at ambient C02 of 35 Pa The Pnamb in control plants of Be, Ah, Ud and Am was about 16, 13, 12 and 5 #mol m -2 s- 1, respectively (Fig. 1), The calculated intercellular CO2 pressure (Ci) differed little among species and was not affected by leaf Mn accumulation (Be, 30+0.3; Ah, 30±0.4; Ud, 28±0.3; Am, 29 + 0.5 Pa). This suggests that stomatal limitation has negligible effect on Pna~b (Sage and Reid, 1994). In all species, P n ~ b decline with increasing leaf Mn concentration. At a Mn level of 3000 #g g - l dry wt above the control (i.e. Be, 1750; Ah, 510; Ud, 150; Am, 130#gg 1dry

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wt Mn), the decline of Pnamb from control was much more modest in the two early successional species of Be (5.3%) and Ah (6.8%) than the mid-successional species of Ud (61%) and late successional species of Am (42%). Carboxylation efficiency Carboxylation efficiency (CE) decreased with increasing leaf Mn concentration in all plants (Fig. 2). Except for Am, CE was about 0.6#real COem-2Pa -1 CO2s -1 in control plants grown at 1 mg litre-I Mn. The CE of Am was about 0.3 #mol CO2 m -2 Pa-] CO2 s-I. When leaf Mn concentration reached 3000/zg g- 1dry wt above the control treatment level of Mn (Be, 1750/zgg -1 dry wt), Ah (510/zgg 1dry wt), Ud (130/zg g-] dry wt) and Am (200 #g g- ] dry wt), CE declined by 4.3, 5.7, 53 and 3 2 0 , respectively. Net photosynthesis at saturating light and CO2 Photosynthesis measured with oxygen electrodes in saturated CO2 and light (Pnsat) was also affected by excess Mn in the leaves (Fig. 3). In control plants, Pnsat of Be, Ah, Ud and Am were about 14, 14, 16 and 14/zmol 02 m -e s- J, respectively. Am and Ud showed considerably higher Pnsat compared with Pnamb in the control treatment. Pnsat declined with increasing leaf Mn concentration in all plants by 1.1% (Be), 4.8% (Ah), 35% (Ud) and 32% (Am) at 3000#gg l dry wt above the lowest Mn levels of 2160/zgg -Idry wt, 1580#gg -1 dry wt, 130#gg -1 dry wt and 130#gg -I dry wt, respectively. Quantum yield The maximum quantum yield of 0 2 evolution (~o2) for Be, Ud and Am in the control treatment was about 0.08 ttmol 02 #mol-~ photon, Ah showed a marginally lower value at about 0.07/zmolO2 #moi -1 (Fig. 4). Manganese accumulation did not have a significant effect on the q~o: of Be. ~o~ of Ah decreased marginally (2.7%) at a leaf Mn concentration 3000 #g g - l dry wt

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Fig. l. Net photosynthesis'of CO2 uptake at ambient CO2 of 35Pa and saturating light (ll00/zmolm -2 s-I PPFD), as affected by leaf Mn accumulation. The measurements were taken on attached, fully-expanded leaves 21-28 days old at the leaf temperature of 25°C. Dotted lines mean 95% confidence intervals. The regression coefficient is significant at p < 0.05 (*) and p < 0.01(**).

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Fig. 4. Effect of leaf Mn accumulation on quantum yield of 02 evolution (~02). *o2 was measured at saturating CO2 (5%) and corrected for leaf absorptance. higher than the minimum observed (1580/xg g-i dry wt). ¢o2 of Ud and A m decreased more significantly with increasing leaf Mn concentration: at 11.6 and 8.9%, respectively, in leaves 3000/zgg -l dry wt above the minimum (Ud, 130; Am, 130/xgg-ldry wt). However, compared with the decline in Pnamb, Pnsat and CE, the decrease in ¢o2 was much more modest.

DISCUSSION

Visible symptoms There was a clear difference among studied species in the level of leaf Mn and the patterns of visible symptoms. Brown spots observed on leaves are typical

symptoms of Mn toxicity and are constituted of Mn oxide and (1,3)-#-glucan (callose) (Horst, 1983; Wissemeier and Horst, 1987). Based on radioautographic studies using 54Mn, heterogeneous distribution of Mn (i.e. brown spots) is typically observed in Mn-sensitive plants while homogeneous distribution with fewer brown spots is seen in Mn-tolerant plants (Horst and Marschner, 1978; Wissemeier and Horst, 1987). In our study, brown spots were observed over the entire leaf of the mid- and late successional species of Ud and Am. In contrast, even at much higher leaf Mn concentrations, the early successional species showed brown spots only in interveinal area (Ah) and the interveinal plus leaf edges (Be), where Mn is known to be preferably accumulated (Romney and Toth, 1954). This suggests that the early successional species of Be and Ah could have more homogeneous Mn distribution in leaves. Homogeneous Mn distribution with fewer brown spots is proposed to be associated with the higher capacity to compartment Mn into vacuoles (Horst and Marschner, 1978; Rufty et al., 1979; Memon and Yatazawa, 1984). It is possible that Be and Ah differ from Ud and A m in vacuole density and capacity but this needs to be further studied.

Photosynthetic response to high leaf Mn The differing sensitivity to Mn toxicity among plant species (Foy et al., 1988) is confirmed by the present study among several tree species native to northern Japan with different successional traits. Based on the responses of Pnamb to leaf Mn accumulation, the early successional species of Be and Ah were tolerant of high Mn while the mid- and late successional species, Ud and Am, were sensitive to excess Mn. Among the parameters of photosynthesis, CE and Pnamb were most affected by high Mn accumulation. Photosynthesis in normal air is limited by both diffusional and biochemical processes. The latter includes the activity of ribulose-l,5-bisphosphate carboxylase/ oxygenase (rubisco) and the regenerative rate of ribulose-l,5-bisphosphate (RuBP) (Sage and Reid, 1994). Although there was little difference in calculated Ci among species, the CO2 concentration at the site of rubisco carboxylation may vary among species through different mesophyll conductance (Sage and Reid, 1994) as inferred from Ames A -l where Ah > Be > Ud> Am (Koike, 1988). For Am, the lowest Ames A -1 associated with low Pnambqn control plants (Fig. 1) may indicate limitations in mesophyll diffusion or in its intrinsic carboxylation potential. If we assume that diffusional limitation due to leaf structure was little changed by high leaf Mn within species, then a decrease in CE (representing the activity of the key photosynthetic enzyme rubisco, Farquhar and Sharkey, 1982; Sharkey, 1985) with high Mn accumulation points to an interference in carboxylation (Fig. 2). Excessive leaf Mn accumulation is reported to affect the activity rather than the amount of rubisco extracted from tobacco leaves (Houtz et al., 1988; McDaniel and Toman, 1994). The activation process of rubisco called 'carbamylation'

Mn toxicity and photosynthesis is known to require CO2 and magnesium (Mg) (Sharkey, 1990). With excessive amounts of Mn in the leaf, the activation o f rubisco by Mg 2÷ could be replace by Mn 2÷ . Because the specificity of Mn2+-rubisco for CO2 versus 02 is lower than that of Mg2+-rubisco by a factor of 20 (Jordan and Ogren, 1981), carbon fixation could be severely curtailed in chloroplasts rich in Mn 2 +-rubisco. Within species, the activity of rubisco appears to be the most important contributor to declining photosynthesis with high leaf Mn, but this may not be the case when comparing among species. Leaf rubisco concentration varies among tree species. Rubisco constitutes the major fraction of leaf nitrogen (Evans, 1989) and has close correlation to light saturated photosynthesis in ambient air (Bj6rkman, 1981). Because higher light saturated photosynthesis is closely associated with higher nitrogen contents (Koike et al., 1992) in early successional species, they may have a larger intrinsic pool of rubisco than mid- and late successional species. Consequently, even with the same concentration of Mn 2 + at rubisco site, early successional species will still retain a greater fraction of functional rubisco activated by Mg 2 ~ to total rubisco. Therefore, higher tolerance to Mn toxicity as expressed through the activity of rubisco may be linked to the inherent pool size of rubisco among species of different successional status. Under saturated CO2 and light, photosynthesis (Pnsat) is regulated by the rate of RuBP regeneration in normal plants (Sharkey, 19851). It is possible that high leaf Mn could have inhibited some processes other than rubisco in the carbon reduction cycle leading to the decreased rate of RuBP regeneration. At saturating CO2, qbo2 derived from the initial slope of photosynthetic light response represents the maximum efficiency of photochemistry after removing the effects of C02 diffusion resistance and photorespiration (Bj6rkman, 1981; Jarvis and Sandford, 1986; Sage and Reid, 1994). In contrast to the decline in the carboxylation activity, maximum photochemical efficiency showed relatively little change even under excess Mn accumulation. It is noteworthy that photosynthetic response to excess Mn is different at low versus high light levels. In low light levels where photosynthesis should be limited not by the activity of carbon metabolism including rubisco activity and RuBP regeneration rate but mainly by the efficiency of photochemistry, M n toxicity is less affected. Seedlings and saplings of mid- and late successional species are generally grown under low light environments such as forest gaps and understory (Koike, 1988). Therefore, such low light environments for juveniles of these species could moderate the effects of Mn toxicity to an extent that remains to be determined.

Different responses among tree species to leaf high Mn Plant species are known to have wide variations in their leaf Mn concentration (Memon et al., 1979). The association between greater accumulation of Mn in

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leaves of horticultural trees and their high Mn tolerance is well established (Aoba, 1986). Similarly, the higher Mn concentrations observed in the early successional species also indicate an associated increase in tolerance, a tolerance reflected in the lack of decline in photosynthesis. The findings presented here on Mn tolerant capacities of four deciduous broad-leaved trees may provide an important criterion for selecting tree species for rehabilitation of the acidic soils in cool temperate forests.

ACKNOWLEDGEMENTS The authors wish to thank Professor S. Sasaki, Professor H. Yagi and Professor T. Tadano for constructive advice, and Dr S. Mori and Dr Y. Maruyama for discussion, and Mr H. Doi for technical support. They are also grateful to Dr K. Satake for helpful suggestions. This work was supported by the Global Environment Research Fund 'Acid Deposition' grant, financed by Japan Environment Agency.

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