Constraints on photosynthesis and antioxidant metabolism in winter and summer crops induced by sulphur dioxide fumigation
Minnaar, Martha Maria
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Recently, major advances have been made in developed countries elucidating the effects of air pollutants on crop plants. In contrast, similar studies on the effects of elevated SO2 concentrations on crops in developing countries such as South Africa are far less advanced. In South Africa, fossil fuel combustion is the main source of energy for most of the country. The tremendous increase in population size and consequental increase in energy demand has lead to considerable increases in fossil fuel burning. This phenomenon has lead to increases in tropospheric air pollutants such as SO2, NO2 and the secondary pollutant, O3. These increases, combined with climatic variations are subject of much concern in agricultural sectors. Fortunately, through many research studies done in European and other developed countries, threshold values have been established for selected crops in an attempt to mitigate the damage done by SO2 and other air pollutants. However, it is with due care that we apply these legislatory thresholds since the environmental conditions in the Southern hemisphere differs greatly from that of the Northern hemisphere. The main aims of this study was firstly to determine the physiological and biochemical basis of SO2 induced inhibition in the C3 and C4 crops, Brassica napus and Zea mays, respectively, and secondly, to study their response with special reference to photosynthesis. The combination of different SO2 levels and induced drought was also investigated. It was hypothesised that SO2 will impair the photosynthetic capacity of both Brassica napus and Zea mays test plants, but that with the addition of drought as co-stress, partial stomatal closure would lead to a mitigation of the SO2-effect on the photosynthetitc apparatus of the mentioned crops. Most of the research that has been done on air pollutants was short term studies, focused on generating dose-response data only over a few weeks of growth. Short term exposures do not answer questions on how initial constraints on photosynthesis could affect crops at a later stage, i.e. how and if these inhibitions affect the yield. In the present study, crops were grown for an entire growth season, from germination until harvest in open-top chambers (OTCs) in an attempt to link early photochemical inhibition to the reduction in yield. OTCs are internationally accepted as the best method to assess the effect of pollutant dosage on crops. Two crops, Brassica napus (C3) and Zea mays (C4) were cultivated and subjected to SO2 enriched air (50,100 and 200 ppb) for eight hours/day, seven days a week. Control plants only received carbon filtered (CF) air. An additional drought treatment was induced in half of the plants of each SO2 treatment. Experiments specifically focussed on the detrimental effect of SO2 on the photosynthetic capacity of the test plants. The photosynthetic capacity was evaluated using chlorophyll a fluorescence induction and photosynthetic gas exchange measurements in parallel, on a weekly basis. Analysis of the OJIP transients provided a number of parameters estimating the energy fluxes and ratios through photosystem II and the intersystem electron transport chain. Gas exchange parameters were deduced from CO2 response curves (A:Ci curves). The ability of the antioxidant metabolism to detoxify reactive oxygen species (ROS) was determined by measuring the POD activity and comparing it to the H2O2 content for Zea mays leaves over a period of nine weeks. Ultimately the cumulative effect of SO2 on the yield was evaluated by determining the shoot mass of Brassica napus and the cob mass of Zea mays. Elevated SO2 concentrations resulted in the partial destruction of chlorophyll pigments, leading to the formation of yellow chlorotic regions in both Brassica napus and Zea mays leaves. These visual effects appeared long after first changes occurred in photosystem II function or photosynthetic gas exchange. In addition to the visual damage, results revealed that elevated SO2 concentrations lead to an impaired photosynthetic capacity in both Brassica napus and Zea mays plants, especially concerning PSII function. The decline in photosynthetic capacity was mainly due to a loss in stomatal functionality, indicated as a reduction in the stomatal conductance for both Brassica napus and Zea mays plants. This was true for well watered and drought stressed treatments in both C3 and C4 crops. The reduced photosynthetic capacity was due to stomatal limitation and to a greater extent, biochemical (mesophyll) limitation. Mespohyll limitation was evident by the decrease in Rubisco activity (Brassica napus: C3) and PEPc activity (Zea mays: C4), in well watered and drought stress treatments. The inability to effectively regenerate ribulosebisphosphate (Brassica napus: C3) and phosphoenolpyruvate (Zea mays: C4) in well watered and drought stressed plants was another mesophyll limitation that contributed to the decline in photosynthesis. By in depth analysis of the chlorophyll a fluorescence transients according to the JIP test, the sites of inhibition in the photosynthetic electron transport chain were elucidated. The changes in the fluorescence transients revealed that the inhibition of the primary processes of photochemistry was mainly due to uncoupling of the oxygen evolving complex in well watered Zea mays and drought stressed Brassica napus plants and to the inhibition of the reduction of end electron acceptors beyond PSI in well watered and drought stressed Brassica napus plants and drought stressed Zea mays test plants. In Zea mays the source of the inhibition of the primary photochemistry through the decline in the reduction of end electron acceptors, was further investigated by in depth analysis of the I-P phase of the OJIP fluorescent transients, i.e. a segment only through photosystem I (PC→RE). The inhibition in well watered and drought stressed treatments were found, not only to be a result of the reduced pool size of electron acceptors, but was also due to a decline in the rate at which end electron acceptors were being reduced. These constraints on the functioning of the photosynthetic electron transport chain were reflected by the inhibition of CO2 assimilation rate, the decline in Rubisco activity (C3 plants) and PEPc anctivity (C4 plants), and decline in the regeneration rate of ribulosebisphosphate (C3 plants) and phosphoenolpyruvate (C4 plants) both due to the decreasing production of reduction equivalents in the light phase. This means that although the fluorescence transients are measured within one second in the dark adapted state, they provide a reliable measure of the whole photosynthetic electron transport chain. SO2 affected both the stomatal function and photosynthetic capacities of Zea mays and Brassica napus. The SO2-related stomatal closure resulted in a decrease in CO2 influx into the leaf and thus a decline in CO2 assimilation. This phenomenon was corroborated by the large decrease in water use efficience in Zea mays and Brassica napus. A marked SO2-concentration dependent decline in the shoot biomass in well watered and drought stressed Brassica napus was evident. Similarly, a reduction in yield occurred in Zea mays test plants, namely reductions in cob mass, in both well watered and drought stressed treatments. The data of the current investigation presented clearly indicate that marked impairment of photosynthesis and yield reduction in the crops, Zea mays and Brassica napus, occured at SO2 concentrations of 50 ppb.These findings proved the first hypothesis of this study to by true in that SO2 adversely affects the photosythetic capacity of crop plants. In Zea mays, more energy was expended towards growth than detoxification of sulphur metabolites. Due to this fact, Zea mays plants still grew to a considerable length with less energy available for cob formation. An increase in H2O2 content due to elevated SO2 concentrations, lead to the degradation of chlorophyll molecules and inhibition of the photosystems which consequentially inhibited the photosynthetic capacity of well watered and drought stressed Zea mays plants. The effectiveness of the antioxidant metabolism to remove H2O2 from mesophyll cells was displayed by the overall decrease in H2O2 content for WW and DS treatments after 9 weeks fumigation. This was achieved by the increased scavenging enzyme activity (increased POD activity) that effectively removed the ROS from the mesophyll cells. Ultimately the data showed that the C3 plant, Brassica napus, was more adversely affected by elevated SO2 concentrations, reducing the photosynthetic assimilation rate greatly. Drought stress however, ameliorated the damaging effect of SO2 on the photosystems to some extent, proving the second hypothesis true for Brassica napus plants. Zea mays plants however showed greater sensitivity towards elevated SO2 concentrations with the addition of drought as a costressor, while amelioration of the inhibitory effect through stomatal closure, proved not to be effective. These findings proved that the second hypothesis was thus only partially proven to be true, and only at low SO2 concentrations for Zea mays crop plants. Within natural environments there may be a magnitude of biotic and abiotic stresses being inposed on crops. The work done in this study is thus of great value to the agricultural sector in early determination of how multiple stressors (SO2 and drought in this case) might affect yield. Management plans can be implemented accordingly. This fact emphasises the magnitude of the relevance and the importance of multiple stress-response studies done on crops, such as the present.