Evolutionary transition from C3 to C4 photosynthesis and the route to C4 rice

Abstract

Compared with C3 plants, C4 plants possess a mechanism to concentrate CO2 around the ribulose-1,5-bisphosphate carboxylase/oxygenase in chloroplasts of bundle sheath cells so that the carboxylation reaction work at a much more efficient rate, thereby substantially eliminate the oxygenation reaction and the resulting photorespiration. It is observed that C4 photosynthesis is more efficient than C3 photosynthesis under conditions of low atmospheric CO2, heat, drought and salinity, suggesting that these factors are the important drivers to promote C4 evolution. Although C4 evolution took over 66 times independently, it is hypothesized that it shared the following evolutionary trajectory: 1) gene duplication followed by neofunctionalization; 2) anatomical and ultrastructral changes of leaf architecture to improve the hydraulic systems; 3) establishment of two-celled photorespiratory pump; 4) addition of transport system; 5) co-option of the duplicated genes into C4 pathway and adaptive changes of C4 enzymes. Based on our current understanding on C4 evolution, several strategies for engineering C4 rice have been proposed to increase both photosynthetic efficiency and yield significantly in order to avoid international food crisis in the future, especially in the developing countries. Here we summarize the latest progresses on the studies of C4 evolution and discuss the strategies to introduce two-celled C4 pathway into rice.

Physiological and comparative proteome analyses reveal low-phosphate tolerance and enhanced photosynthesis in a maize mutant owing to reinforced inorganic phosphate recycling

“…The “CO 2 pump” mechanism in C4 plants increases the level of CO 2 around RuBisCO, which may increase the carboxylation reaction rate and reduce the alternative fixation of O 2 . C4 photosynthesis is more efficient than C3 photosynthesis under low atmospheric CO 2 conditions, which suggests that the “CO 2 pump” is an important mechanism that leads to an increase in photosynthesis [ 30 ]. The accumulation and activity levels of NADP-ME and PPDK were higher in Qi319-96 than in Qi319 under phosphate deprivation conditions, which favored a greater capture rate and level of CO 2 in vascular bundle sheath cells.…”

Molecular adaptation in Rubisco: Discriminating between convergent evolution and positive selection using mechanistic and classical codon models

“…However, under present atmospheric conditions (lower CO 2 and higher O 2 concentration), photorespiration can represent a significant proportion of the enzymatic activity of Rubisco, such that the efficiency of photosynthesis can be dropped by 40% under unfavorable climates like hot and dry conditions [ 4 ]. As a result, some plants have developed an evolved improvement to C3 pathway called C4 photosynthesis as an adaptation to these changes in the environment [ 5 , 6 ].…”

Progress and prospects of C4 trait engineering in plants

“…Despite many attempts at generating C 4 rice transgenics, higher photosynthate assimilation is yet to be achieved, which is the major focus of C 4 rice development. The photorespiratory pathway must be reorientated to achieve higher carboxylation of RuBisCo (Liu et al 2013). Using C 4 pathway enzymes, firstgeneration C 4 rice has been achieved, but even all five enzymes described above proved inadequate for development of C 4 rice (Ermakova et al 2020).…”

“…Using C 4 pathway enzymes, firstgeneration C 4 rice has been achieved, but even all five enzymes described above proved inadequate for development of C 4 rice (Ermakova et al 2020). This has also revealed the importance of M and BS cell-specific intracellular metabolite transport (Liu et al 2013). The advent of next-generation sequencing technology and proteomics approaches identified many metabolic transporter proteins that could be utilized for transgenic development through cloning the corresponding genes from a C 4 plant, like maize.…”

“…The photorespiratory pathway must be reorientated to achieve higher carboxylation of RuBisCo (Liu et al . 2013). Using C 4 pathway enzymes, first‐generation C 4 rice has been achieved, but even all five enzymes described above proved inadequate for development of C 4 rice (Ermakova et al .…”