Mild water stress, on the order of -1.0 megapascals xylem water potential, can reduce the rate of photosynthesis and eliminate the inhibition of photosynthesis caused by 02 in waterstress-sensitive plants such as Phaseolus vulgaris. To investigate the lack of 02 inhibition of photosynthesis, we measured stromal and cytosolic fructose-1,6-bisphosphatase, sucrose phosphate synthase, and partitioning of newly fixed carbon between starch and sucrose before, during, and after mild water stress. The extractable activity of the fructose bisphosphatases was unaffected by mild water stress. The extractable activity of SPS was inhibited by more than 60% in plants stressed to water potentials of -0.9 megapascals. Water stress caused a decline in the starch/sucrose partitioning ratio indicating that starch synthesis was inhibited more than sucrose synthesis. We conclude that the reduced rate of photosynthesis during water stress is caused by stomatal closure, and that the restriction of CO2 supply caused by stomatal closure leads to a reduction in the capacity for both starch and sucrose synthesis. This causes the reduced 02 inhibition and abrupt CO2 saturation of photosynthesis.Mild water stress, on the order of -1.0 MPa, can reduce the rate of photosynthesis in water-stress-sensitive plants such as Phaseolus vulgaris. The reduced rate of photosynthesis can be caused by stomatal closure or by direct effects of water stress on the biochemical reactions of photosynthesis. Two possible sites of water stress damage to the biochemistry of photosynthesis are (a) reactions associated with the thylakoid membranes (2), and (b) stromal reactions associated with the photosynthetic carbon reduction cycle especially the carboxylation reactions (8). Farquhar and Sharkey (5) argued that since the response of photosynthesis to intercellular CO2 partial pressure was reduced, there must be some effect of mild water stress on the biochemical reactions of photosynthesis. This argument is now suspect because it has been found that stomata can close more over some sections of the leaf than over other sections (patchy closure). The patchy stomatal closure was first seen in response to feeding abscisic acid (4,26) and has been demonstrated in water-stressed Phaseolus leaves (21).Kaiser (7) isolated chloroplasts and that the loss of photosynthesis in leaves resulting from water stress is probably caused by stomatal closure and direct effects on the partial pressure of CO2 within the leaf. In addition, Sharkey and Seeman (21) showed that carbamylation of RuBPCase, kca of RuBPCase, and RuBP pool size was not affected by a mild water stress (-0.7 MPa) even though the rate of photosynthesis was reduced by 75%. Similar results have been obtained with abscisic acid fed leaves (17). Only small effects on these parameters were seen in leaves with a water potential of -1.1 MPa, even though photosynthesis was almost completely eliminated by this degree of water stress. Sharkey and Seeman (21) concluded that the reduction in photosynthesis caused by...
J.M. Keller et al. (1989, EMBO J. 8, 1005-1012) introduced a phytochrome gene controlled by a cauliflower mosaic virus 35S promoter into tobacco (Nicotiana tabacum L.) providing material to test whether several photosynthesis enzymes can be increased by one modification to the plant. We report here that this transgenic tobacco had greater amounts of all enzymes examined as well as greater amounts of total protein and chlorophyll per unit leaf area. Fructose bisphosphatase (E.C. 3.1.3.11), glyceraldehyde 3-phosphate dehydrogenase (E.C. 1.2.1.12), and sucrose-phosphate synthase (E.C. 2.4.1.14) were also higher when expressed per unit protein. However, ribulose-1,5-bisphosphate carboxylase (E.C. 4.1.1.39) amount per unit leaf protein was the same in transgenic and wild-type (WT) plants. Photosynthesis in the transgenic plants was lower than in WT at air levels of CO2, but higher than in WT above 1000 μbar CO2. The photosynthesis results indicated a high resistance to CO2 diffusion in the mesophyll of the transgenic plants. Examination of electron micrographs showed that chloroplasts in the transgenic plants were often cup-shaped, preventing close association between chloroplast and cell surface. Chloroplast cupping may have caused the increase in the mesophyll resistance to CO2 diffusion. We conclude that it is possible to affect more than one enzyme with a single modification, but unexpected physical modifications worsened the photosynthetic performance of this plant.
Photosynthesis of C3 plants is occasionally inhibited upon switching from normal to low partial pressure of 02. Leaves of Solanum tuberosum exhibited this effect reproducibly under saturafing light and 700 microbars of CO2. We determined the partitioning of recent photosynthate between starch and sucrose and measured the concentration of hexose monophosphates in the stroma and cytosol after nonaqueous fractionation. The reduction in the rate of photosynthesis upon switching to low partial pressure of 02 was caused by reduced starch synthesis. The concentration of hexose monophosphates in the stroma fell and the glucose 6-phosphate to fructose 6-phosphate to fructose 6-phosphate ratio fell from 2.7 to 1.3, indicating an inhibition of phosphoglucoisomerase as described by K-J Dietz ([1985] Biochim Biophys Acta 839: 240-248). The concentration of hexose monophosphates in the cytosol increased, ruling out a sucrose synthesis limitation by reduced transport from the chloroplast as the explanation for low 02 inhibition of photosynthesis.Oxygen usually inhibits photosynthesis ofC3 plants because of photorespiration. Sometimes, photosynthesis of C3 plants can be insensitive to 02; switching to low 02 partial pressure causes no change in the rate of photosynthesis (1 1). Oxygen insensitivity is believed to result from a feedback limitation of photosynthesis ( 15). Occasionally, photosynthesis is inhibited by switching to low 02 partial pressure (1,2,7,8,16 The mechanism of reduced starch synthesis described by Dietz (3) works like this. PGA inhibits phosphoglucoisomerase, the enzyme necessary for conversion of F6P to G6P. At low rates of photosynthesis this effect is overshadowed by the stimulatory effect of PGA on ADPglucose pyrophosphorylase (9). However, as the rate of photosynthesis increases, and the concentration of PGA increases, the inhibition of phosphoglucoisomerase is observed as a displacement from equilibrium ofthe G6P/F6P ratio. While this ratio is usually 3, it falls to 1.3 in chloroplasts at high rates of photosynthesis (3,5). Dietz showed that starch accumulation was reduced in low 02 concentration when the G6P/F6P ratio was low.The three explanations for low 02 inhibition of photosynthesis can be distinguished on the basis of their effect on partitioning to starch and sucrose. Ifelectron transport effects are responsible, then little effect on partitioning between starch and sucrose is expected. If inhibited sucrose synthesis is responsible, then it is expected that less photosynthate will be partitioned into sucrose and more into starch. But if the effect described by Dietz (3) is responsible, then less photosynthate is expected in starch at low 02 partial pressure than at normal 02 partial pressure.We have measured the partitioning of recent photosynthate between starch, sucrose, and the ionic fraction in potato leaves in normal and low 02 partial pressure under conditions which caused the low 02 inhibition of photosynthesis. We also measured the concentration of F6P and G6P in the stroma and...
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