Effects of sulphur dioxide on photosynthesis in the succulent Augea capensis Thunb
Introduction
Although emissions of sulphur dioxide (SO2), a phytotoxic by-product of fossil fuel burning, have decreased considerably in North America and Europe (Cape et al., 2003), the opposite is unfortunately true in many developing countries (Agrawal and Deepak, 2003). SO2 can cause positive effects on physiological and growth characteristics of plants at very low concentrations, especially in sulphur-deficient soils (Darrall, 1989). Mostly, however, increased uptake of SO2 causes toxicity and reduced growth and productivity due to accumulation of sulphite and sulphate within the plant. The main factors that determine the phytotoxicity of SO2 are: environmental conditions, duration of exposure, atmospheric SO2 concentration, sulphur status of the soil and the genetic constitution of the plant (Saxe, 1991).
SO2 can enter leaves as readily as CO2 through the stomata. Even if the stomata are closed, SO2 can still enter the leaf by overcoming the cuticular resistance (Larcher, 2003). The solubility factor of SO2 is almost 40 times higher than that of CO2 making it a stronger acid (Pfanz and Heber, 1986). This enables SO2 to dissolve in the apoplast leading to the formation of hydrogen sulphite (HSO3−) and sulphite (SO32−), which then enters the cell (Larcher, 2003).
Both the visual symptoms and biochemical effects of SO2 on plants are well documented (e.g., Rakwal et al., 2003). At the pH within the chloroplast, SO2 is mainly converted to sulphite, which is know to inhibit: (i) CO2 assimilation, (ii) stromal bisphosphatase activity, (iii) ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activity, (iv) photophosphorylation and (v) the operation of the triose-phosphate translocator (Cerovic et al., 1982; Larcher, 2003; Mourioux and Douce, 1979). With increasing SO2 concentration, an increased inhibition of photosynthetic enzymes is known to occur (Veljovic-Jovanovic et al., 1993). Nieboer et al. (1976) also found that SO2 and its oxidation products are capable of interfering with photosynthetic electron transport thereby restricting the supply of reducing equivalents required for reductive carbon metabolism.
Because harmful atmospheric SO2 concentrations most frequently occur in and around heavily industrialised areas, previous studies have focused mainly on the impacts of SO2 on typical vegetation occurring in these environments. In contrast, the impacts of SO2 pollution on succulent species occurring in arid environments are relatively unknown, mainly because vegetation in these areas is seldom exposed to SO2 pollution due to limited anthropogenic activities and distance from industrialised point sources. The few studies that have investigated effects of SO2 on vegetation in arid environments focused on species with crassulacean acid metabolism (CAM) (e.g., Olszyk et al., 1987) or desert winter annuals and perennials (Thompson et al., 1984). The unique metabolic adaptations in CAM plants allow for nocturnal stomatal opening, which is a very important survival mechanism in arid environments (Ting, 1985). However, these adaptations make it difficult to extrapolate findings about air pollution effects in CAM plants to succulent species with typical C3-mode CO2 assimilation.
The need for additional information about the effects of SO2 pollution on desert vegetation arose recently when Skorpion Zinc mine and refinery started operation during 2003 in the southwestern region of the Namib Desert (Namibia). Sulphuric acid, used during the zinc refinery process, is produced in an acid plant at the refinery, and under normal operating conditions very low concentrations of SO2, generally not considered to be phytotoxic, are emitted to the atmosphere. However, the potential effects on vegetation in the event of higher SO2 concentrations being emitted are not known and were investigated in this study. Skorpion Zinc mine and refinery is situated inside the so-called Sperrgebiet (forbidden area), an area that has virtually been undisturbed because of highly restricted access due to diamond mining along the Atlantic coastline approximately 60 km to the west. This region of the Namib Desert falls within the northern boundaries of the Succulent Karoo biome, which is regarded as a global biodiversity hotspot because of exceptionally high plant species diversity (Cowling et al., 1999).
In this paper, we report on a series of experiments, conducted under controlled growth conditions, that investigated the effects of SO2 on Augea capensis Thunb., a succulent species exhibiting C3-mode photosynthesis that occurs in abundance at Skorpion Zinc mine. Because of the central role of carbon metabolism in plant productivity, the investigation focused on the effects of SO2 on photosynthesis. Effects were assessed by means of CO2 assimilation and chlorophyll a fluorescence measurements. In addition, we propose a possible explanation for observed diurnal (day versus night) differences in SO2 sensitivity in this species.
Section snippets
Plant material and growth conditions
A. capensis Thunb. (family Zygophyllaceae), an evergreen succulent with fleshy cylindrical leaves and stems (Fig. 1), was selected for all laboratory experiments, mainly because of its widespread occurrence at Skorpion Zinc mine (Rosh Pinah, Namibia) and high survival rates following transplantation to pots. Young specimens (maximum 20 cm in height) were excavated from the desert in the vicinity of the mine and transplanted into 15 d m3 plastic pots containing desert soil. Potted plants were
Inhibition of CO2 assimilation by SO2 fumigation in the light
For the purpose of determining the relative sensitivity of A. capensis to SO2 in the fumigation system employed in this investigation, soybean was used as an indicator species because of its well-characterised phytotoxic response to SO2. A single day of SO2 fumigation at a concentration of 1.2 ppm in the light led to discolouring of leaves and curling of leaf margins in more than 70% of all leaves in treated soybean plants. These symptoms were progressively manifested in all leaves and
Discussion
The sensitivity of plants to SO2 pollution is well described in the scientific literature. Even at low concentrations of between 0.06 and 0.15 ppm reduced growth and yield, decreased foliar starch and protein content, pigment loss and a decrease in water use efficiency are frequently observed (e.g., Deepak and Agrawal, 2001; Verma and Agrawal, 1996). Keeping this in mind, severe inhibition of most aspects of plant function was expected at the highest concentration of 1.2 ppm used in our
Acknowledgements
We acknowledge Namzinc (Pty) Ltd. for full financial support of this project and North-West University (Potchefstroom, South Africa) for the provision of research facilities and equipment. Mr. O. Pretorius (Chief Environmental Technician, Environment Synfuels, SASOL, South Africa) provided the SO2 analyser used in all experiments. The National Research Foundation (NRF) of South Africa provided a postgraduate bursary to J.W. Swanepoel.
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