Photorespiration and Its Consequences

The enzyme rubisco, used by the Calvin-Benson cycle to fix CO₂ during photosynthesis, is probably the most abundant enzyme on the planet. Its properties are remarkably identical in all photosynthetic organisms, from bacteria to flowering →follows, we will identify and explore some of these limitations and see how evolution has constructed metabolic bypasses around them. First we’ll look at photorespiration, a process in which rubisco reacts with O₂ instead of CO₂, lowering the overall rate of CO₂ fixation. Then we’ll examine some biochemical pathways and features of plant anatomy that compensate for the limitations of rubisco.

Rubisco catalyzes RuBP reaction with O2 as well as CO₂

As its full name indicates, rubisco is a carboxylase(addingCalvin–Benson cycle. The phosphoglycolate forms glycerate which diffuses into membrane-enclosed organelles called peroxisomes. There, a series of reactions converts it to the amino acid glycine: glycolate →→glycine The glycine then diffuses into a mitochondrion, where two glycine molecules are converted to glycerate (a three-carbon molecule), and CO₂: 2 glycine →glycerate + CO₂ This pathway is called photorespirationbecause it consumes O₂ and releases CO₂. It uses ATP and NADPH produced in the light reactions, just like the Calvin–Benson cycle. The net effect is to take two two-carbon molecules and make one threecarbon molecule. So one carbon of the four is released as CO₂ and three of the carbons (75%) are recovered as fixed carbon. In other words, photorespiration reduces net carbon fixation by 25 percent compared with the Calvin–Benson cycle. How does rubisco “decide” whether to act as an oxygenase or a carboxylase? First, rubisco has 10 times more affinity for CO₂ than O₂, and so favors CO₂ fixation. Another consideration is the relative concentrations of CO₂ and O₂ in the leaf. If O₂ is relatively abundant, rubisco acts as an oxygenase, and photorespiration ensues. If CO₂ predominates, rubisco fixes it and the Calvin–Benson cycle occurs. Temperature is also a factor: photorespiration is more likely at high CO₂ to the acceptor molecule RuBP) as well as an oxygenase (adding O₂ to RuBP). These two reactions compete with each other. So when RuBP reacts with O₂, it cannot react with CO₂. This reaction reduces the overall CO₂ that is converted to carbohydrates, and therefore limits plant growth. When O₂ is added to RuBP, one of the products is a twocarbon compound, phosphoglycolate: RuBP + O₂ →phosphoglycolate + 3PG Plants have evolved a metabolic pathway that partially recovers the carbon that has been channeled away from the temperatures.

Rubisco acts as an oxygenase, and photorespiration occurs, under these conditions. Because the first product of CO₂ fixation in these plants is the three-carbon molecule 3PG, they are called C3 plants. Corn, sugarcane, and other tropical grasses also close their stomata on a hot day, but their rate of photosynthesis does not fall, nor does photorespiration occur. They keep the ratio of CO₂ to O₂ around rubisco high so that rubisco continues to act as a carboxylase. They do this in part by making a four-carbon compound, oxaloacetate, as the first product of CO₂ fixation, and so are called C4 plants. C4 plants perform the normal Calvin–Benson cycle, but they have an additional early reaction that fixes CO₂ without losing carbon to photorespiration, greatly increasing the overall photosynthetic yield. Because this initial CO₂ fixation step can function even at low levels of CO₂ and high temperatures, C4 plants very effectively optimize photosynthesis under conditions that inhibit it in C3 plants. C4 plants have two separate enzymes for CO₂ fixation located in two different parts of the leaf (Figure ). One enzyme, present in the cytosol of mesophyll cells near the surface of the leaf, fixes CO₂ to a three-carbon acceptor compound, phosphoenolpyruvate (PEP), to produce the fourcarbon fixation product, oxaloacetate. This enzyme, PEP carboxylase, has two advantages over rubisco:

It does not have oxygenase activity.

It fixes CO₂ even at very low CO₂ levels.

So even on a hot day when the stomata are closed, the CO₂ concentration in the leaf is low, and the O₂ concentration is high, PEP carboxylase just keeps on fixing CO₂. Oxaloacetate diffuses out of the mesophyll cells and through plasmodesmata into the bundle sheath cells, located in the interior of the leaf. The chloroplasts in bundle sheath cells contain abundant rubisco. There, the four-carbon oxaloacetate loses one carbon, forming CO₂ and regenerating the threecarbon acceptor compound, PEP, in the mesophyll cells. Thus, the role of PEP is to bind CO₂ from the air in the leaf and carry it to the bundle sheath cells, where it is “dropped off” at rubisco. This process essentially pumps up the CO₂ concentration around rubisco, so that it acts as a carboxylase and begins the Calvin–Benson cycle. Kentucky bluegrass, a C3 plant, thrives on lawns in April and May. But in the heat of summer, it does not do as well, and crabgrass, a C4 plant, takes over the lawn. The same is true on a global scale for crops: C3 plants, such as soybeans, rice, wheat and barley, have been adapted for human food production in temperate climates, while C4 plants, such as corn and sugarcane, originated and are grown in the tropics. C3 plants are certainly more ancient than C4 plants. While C3 photosynthesis appears to have begun about 3.5 billion years ago, C4 plants appeared about 12 million years ago. A possible factor in the emergence of the C4 pathway is the decline in atmospheric CO₂. When dinosaurs ruled Earth 100 million years ago, the concentration of CO₂ in the atmosphere was four times what it is now. As CO₂ levels declined thereafter, the more efficient C4 plants would have had an advantage over their C3 counterparts.

CAM plants also use PEP carboxylase

Other plants besides the C4 species use PEP carboxylase to fix and accumulate CO2. Such plants include some water-storing plants (called succulents) of the family Crassulaceae, many cacti, pineapples and several other kinds of flowering plants. The CO₂ metabolism of these plants is called crassulacean acid metabolism, or CAM, after the family of succulents in which it was discovered. CAM is much like the metabolism of C4 plants in that CO₂ is initially fixed into a four-carbon compound. In CAM plants, however, the processes of initial CO₂ fixation and the Calvin–Benson cycle are separated in time, rather than in space.

At night, when it is cooler and water loss in minimized, the stomata open. CO₂ is fixed in mesophyll cells to form the four-carbon compound oxaloacetate which is converted to malic acid.

During the day, the accumulated malic acid is shipped to the chloroplasts, where decarboxylation supplies the CO₂ for operation of the Calvin–Benson cycle and the light reactions supply the necessary ATP and NADPH + H+.