Rubisco oxygenase activity

Photorespiration Results from Rubisco s Oxygenase Activity... 

FIGURE 20-20 Oxygenase activity of rubisco. Rubisco can incorporate 02 rather than C02 into ribulose 1,5-bisphosphate. The unstable intermediate thus formed splits into 2-phosphoglycolate (recycled as described in Fig. 20-21) and 3-phosphoglycerate, which can reenter the Calvin cycle. 

The combined activity of the rubisco oxygenase and the glycolate salvage pathway consumes 02 and produces C02—hence the name photorespiration. This pathway is perhaps better called the oxidative photosynthetic carbon cycle or C2 cycle, names that do not invite comparison with respiration in mitochondria. Unlike mitochondrial respiration, photorespiration does not conserve energy and may actually inhibit net biomass formation as much as 50%. This inefficiency has led to evolutionary adaptations in the carbon-assimilation processes, particularly in plants that have evolved in warm climates. 

The PEP carboxylase of mesophyll cells has a high affinity for HCCU (which is favored relative to C02 in aqueous solution and can fix C02 more efficiently than can rubisco). Unlike rubisco, it does not use 02 as an alternative substrate, so there is no competition between C02 and 02. The PEP carboxylase reaction, then, serves to fix and concentrate C02 in the form of malate. Release of C02 from malate in the bundle-sheath cells yields a sufficiently high local concentration of C02 for rubisco to function near its maximal rate, and for suppression of the enzyme s oxygenase activity. 

N. E. Tolbert4 has argued that the dual specificity of rubisco for C02 and 02 is not simply a leftover from evolution in a low-oxygen environment. He suggests that the relative activities of the carboxylase and oxygenase activities of rubisco actually have set, and now maintain, the ratio of C02 to 02 in the earth s atmosphere. Discuss the pros and cons of this hypothesis, in molecular terms and in global terms. How does the existence of C4 organisms bear on the hypothesis ... 

At 30°C and for an absorbed PPF up to about 100 jimol m-2 s-1, leaves of C3 and C4 plants can have a similar quantum yield (approximately 0.053 mol CCh/mol photons at an of 325 pmol mol-1 Fig. 8-20 Ehleringer and Bjorkman, 1977 see Chapter 4, Section 4.4B for a definition of quantum yield). As the temperature is raised, however, photorespiration increases relative to photosynthesis, so the quantum yield declines for C3 plants but is essentially unchanged for C4 plants. On the other hand, lowering the ambient O2 level raises the quantum yield for C3 (photorespiring) plants because the oxygenase activity of Rubisco (see Fig. 8-13) is then suppressed such changes have little effect on C4 plants until the 02 level falls below about 2%, where mitochondrial respiration is affected. 

The most prominent side reaction of Rubisco is its counterproductive oxygenase activity, reflecting competition with CO2 for the enediol(ate) intermediate (1) (23). Partitioning between the two pathways (vjvo) is defined by Vc/Vo = T ([C02]/[02]), where x is VJCJVoK,. (24). Because x can be interpreted in terms of the free energy differential for carboxylated versus oxygenated transition states (25-26), it provides insight into determinants of Rubisco specificity. 

The oxygenase activity of rubisco increases with temperature. Crabgrass is a C4 plant, whereas most grasses lack this capability. Consequently, the crabgrass will thrive at the hottest part of the summer because the C4 pathway provides an ample supply of CO2. 

Concurrently to the assimilation in leaves there is always CO2 production in respiration and photorespiration (the first occurs all the time and involves the mitochondria, the latter occurs only in the light and involves also the oxygenase activity of Rubisco in the chloroplasts). Any discrimination in the respiration process will be reflected in the isotopic composition of the CO2 produced and mixed into the leaf internal CO2 pool and its effect must, therefore, be subtracted from Ap. The combined effect of the two respiratory components can be subtracted from Equation (24) as (Farquhar and Lloyd, 1993 Farquhar et al., 1982)... 

C4 photosynthesis is an adaptation to growth in hot climates. The first products of photosynthesis are C4 acids normal plants produce PGA, a 3 carbon acid, and hence are termed C3 plants. C4 photosynthesis has evolved independently in at least 16 families of flowering plemts. C4 metabolism is a way of getting round the problem of Rubisco s unfortunate oxygenase activity. C4 plants concentrate CO2 biochemically in a variety of ways, so Rubisco is exposed to a very high CO2/O2 ratio, which inhibits photorespiration. 

This salvage pathway serves to recycle three of the four carbon atoms of two molecules of glycolate. However, one carbon atom is lost as CO2. This process is called photorespiration because O2 is consumed and CO2 is released. Photorespiration is wasteful because organic carbon is converted into CO2 without the production of ATP, NADPH, or another energy-rich metabolite. Evolutionary processes have presumably enhanced the preference of rubisco for carboxylation. For instance, the rubisco of higher plants is eightfold as specific for carboxylation as that of photosynthetic bacteria. However, some oxygenase activity may be an inevitable side effect of the carboxylase reaction mechanism. 

Under conditions of high temperature, the carbon dioxide compensation point of C3 plants rises because the oxygenase activity of Rubisco increases more rapidly than the carboxylase activity. 

The C isotopic record provides support for the greatly diminished C02 and elevated 02 atmospheric concentrations (Beerling et al. 2002).The evidence arises from the fact that the enzyme rubisco catalyses both photosynthetic carboxylation and photorespirational oxidation. Consequently, C02 and 02 compete for acceptor molecules of the enzyme. So if pC02 rises the oxygenase activity of rubisco is suppressed, and conversely ifp02 rises the carboxylase activity of rubisco is... 

Rubisco is not absolutely specific for CO2 as a substrate. Molecular oxygen (O2) competes with CO2 at the active site, and about once in every three or four turnovers, rubisco catalyzes the condensation of O2 with ribulose 1,5-bisphosphate to form 3-phosphoglycerate and 2-phosphoglycolate (Fig. 20-20), a meta-bolically useless product. This is the oxygenase activity referred to in the full name of the enzyme ribulose... 

Unlike ribulose bisphosphate carboxylase (rubisco) from the Calvin cycle, phosphoenolpyruvate carboxylase has no oxygenase activity. As a result, capturing C02 into oxaloacetate serves as a mechanism for delivering C02 to the Calvin cycle process in the bundle sheath cells, not for initiating photorespiration. In this way, high levels of C02 can be maintained in the bundle sheath cells, favoring C02 fixation rather than photorespiration. Even if photorespiration does occur, C02 released in that process may be readily returned to the Calvin cycle by the C4 pathway, instead of being lost. 

The reaction, which occurs in C4 plants and bacteria, uses the high energy phosphate of PEP to drive the incorporation of a carboxyl group in order to form oxaloacetate. In C4 plants, PEP carboxylase is located in the mesophyll cells on the external surfaces of the plant. Incorporation of C02 in this manner helps to shuttle C02 to the bundle sheath cells, where the Calvin cycle enzymes are concentrated. It also helps to avoid the wasteful photorespiration cycle due to the oxygenase activity of the C02 fixing enzyme, rubisco. 

Recall that the oxygenase activity of rubisco increases more rapidly with temperature than does its carboxylase activity. How then do plants, such as sugar cane, that grow in hot climates prevent very high rates of wasteful photorespiration Their solution to this problem is to achieve a high local concentration of CO2 at the site of the Calvin cycle in their photosynthetic cells. The essence of this process, which was elucidated by M. D. Hatch and C. R. Slack, is that four-carbon (Cfi compounds such as oxaloacetate and malate carry CO2 from mesophyll cells, which are in contact with air, to bundle-sheath cells, which are the major sites of photosynthesis (Figure 20.17). Decarboxylation of the four-carbon compound in a bundle-sheath cell maintains a high concentration of CO2 at the site of the Calvin cycle. The three-carbon compound pyruvate returns to the mesophyll cell for another round of carboxylation. 

Most plants would be more productive in the absence of photorespiration. There is another side to this picture, however. The oxygenase activity appears to be an unavoidable, wasteful activity of rubisco. Photorespiration is a salvage pathway that saves some of the carbon that would be lost due to the oxygenase activity of rubisco. Photorespiration is essential to plants even though the plant pays the price in loss of ATP and reducing power mutations that affect this pathway can be lethal. 

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