Poales - Missouri Botanical Garden

If the C4 cycle is superimposed onto a C2 cycle operating in a C3–C4 intermediate plant, the C2 photosynthesis model predicts a mechanistic interaction between the C2 and C4 cycles (). When the C4 cycle is running, the photorespiratory ammonia is recirculated from the bundle sheath to the mesophyll cells by moving malate from the mesophyll to the bundle sheath and transferring alanine back to the mesophyll. This malate/alanine cycling leads to a net transport of ammonia from the bundle sheath into the mesophyll cells. In contrast to the other mechanisms of ammonia recirculation described above, the C4 cycle does not only lead to a net transport of ammonia from the bundle sheath to the mesophyll but additionally also to a net transport of CO2 in the opposite direction. Thus CO2 is transferred from the mesophyll to the bundle sheath without increasing the number of transport processes between the cells. By elevating the CO2 concentration in the bundle sheath cells the C4 cycle acts cooperatively with the C2 cycle. The bundle sheath Rubisco would work under a more elevated CO2 concentration and thus operate more effectively compared to a pure C2 plant, leading to an increased biomass production. The C4 cycle thus has a dual beneficial effect: an efficient nitrogen shuttle is combined with a CO2 concentrating pump.

What happens during photorespiration.

As shown in Figure 2 (left), RuBisCO is one of many enzymes in the Calvin cycle

2 and CO 2 on the Rubisco enzyme of the Calvin-Benson cycle

To study the evolution of the expression of photorespiratory and C4 cycle genes during the transition from C3 to C4 photosynthesis in the genus Flaveria, nine species reflecting the evolutionary trajectory taken were selected, including two C3 (F. robusta and F. pringlei), two C4 (F. bidentis and F. trinervia), and five C3–C4 intermediate species (). According to their CO2 compensation points and the percentage of carbon initially fixed into malate and aspartate, F. chloraefolia and F. pubescens were earlier classified as type I C3–C4 intermediates. F. anomala and F. ramosissima belong to the type II C3–C4 intermediates and F. brownii is classified as a C4-like species (; ; ; ). Type I C3–C4 intermediates are defined as solely relying on the photorespiratory CO2 concentration cycle whereas a basal C4 cycle activity is present in type II C3–C4 intermediates species. C4-like species exhibit much higher C4 cycle activities but lack complete bundle sheath compartmentation of Rubisco activity ().

What is the role of rubisco in the Calvin Cycle

In hot and dry environments and under low atmospheric CO2 conditions, when the oxygenation activity of Rubisco is increased, the high rate of photorespiration becomes unfavorable for the plants (, ). C4 plants possess a mechanism that minimizes the oxygenase function of Rubisco and thereby reduces photorespiration and decreases the loss of carbon. C4 photosynthesis is based on a division of labor between two different cell types, mesophyll and bundle sheath cells, which are organized in a wreath-like structure called ‘Kranz Anatomy’ (; ). Atmospheric CO2 is initially fixed in the mesophyll by phosphoenolpyruvate carboxylase (PEPC), and the resulting four-carbon compound is transported to the bundle sheath cells and decarboxylated by NADP/NAD malic enzyme or phosphoenolpyruvate carboxykinase (). Thereby CO2 is concentrated at the site of the Rubisco in the bundle sheath cells (), outcompeting the molecular oxygen. As a consequence, photorespiration is drastically reduced as compared to C3 plants, and C4 plants are characterized by a high photosynthetic efficiency ().

in the Calvin–Benson cycle, but ..

C4 photosynthesis represents a most remarkable case of convergent evolution of a complex trait, which includes the reprogramming of the expression patterns of thousands of genes. Anatomical, physiological, and phylogenetic and analyses as well as computational modeling indicate that the establishment of a photorespiratory carbon pump (termed C2 photosynthesis) is a prerequisite for the evolution of C4. However, a mechanistic model explaining the tight connection between the evolution of C4 and C2 photosynthesis is currently lacking. Here we address this question through comparative transcriptomic and biochemical analyses of closely related C3, C3–C4, and C4 species, combined with Flux Balance Analysis constrained through a mechanistic model of carbon fixation. We show that C2 photosynthesis creates a misbalance in nitrogen metabolism between bundle sheath and mesophyll cells. Rebalancing nitrogen metabolism requires anaplerotic reactions that resemble at least parts of a basic C4 cycle. Our findings thus show how C2 photosynthesis represents a pre-adaptation for the C4 system, where the evolution of the C2 system establishes important C4 components as a side effect.

of O 2 that are taken up by RuBisCO

In C3 plants, basal activities of the typical C4 cycle enzymes are present (). When our integrated model is parameterized to include an active C4 cycle, it predicts that a contingent of the bundle sheath ammonia will be transferred to the mesophyll cells by the C4 cycle as a biomass neutral alternative to the 2-OG/Glu shuttle or as the unique solution when additional weight on plasmodesmatal fluxes is applied (). In this solution malate is decarboxylated in the bundle sheath cells. CO2 is refixed by Rubisco, and the resulting pyruvate is aminated by Ala-AT. Alanine moves to the mesophyll cells, where ammonia is fed into the photorespiratory cycle by Ala-AT and GGT. The resulting pyruvate is converted back to malate by PPDK, PEPC, and NADPH-dependent MDH (). Flux variability analysis shows that only marginal variability in the fluxes of the shuttle is possible (). According to our model predictions, the cycle is active even at low PEPC activities, such as those measured in C3Flaveria species (; ). When the C4 cycle runs with low capacity, according the model, the surplus of bundle sheath ammonia is transferred back to the mesophyll by the glutamate/2-oxoglutarate shuttle. Once the capacity of the C4 cycle gradually increases, the recirculation of nitrogen is shifted from the glutamate/2-oxoglutarate shuttle towards the C4 cycle (). The predicted biomass production increases linearly with C4 cycle activity (). Thus, our model predicts a strong interaction between C2 and C4 photosynthesis.

tions to both photosynthesis and photorespiration ..

In photorespiration, oxygen reacts with the ribulose-1,5-bisphosphate to reverse carbon fixation in the Calvin Cycle and thus, reduces the efficiency of photosynthesis.