Can improved canopy light transmission ameliorate loss of photosynthetic efficiency in the shade? An investigation of natural variation in Sorghum bicolor.

Previous studies have found that maximum quantum yield of CO2 assimilation (ΦCO2,max,app) declines in lower canopies of maize and Miscanthus, a maladaptive response to self-shading. These observations were limited to single genotypes, leaving it unclear that the maladaptive shade response is a general property of this C4 grass tribe, the Andropogoneae. We explored the generality of this maladaptation by testing the hypothesis that erect leaf forms (erectophiles), which allow more light into the lower canopy, suffer less of a decline in photosynthetic efficiency than drooping leaf (planophile) forms. On average, ΦCO2,max,app declined 27% in lower canopy leaves across 35 accessions, but the decline was over twice as great in planophiles than in erectophiles. The loss of photosynthetic efficiency involved a decoupling between electron transport and assimilation. This was not associated with increased bundle sheath leakage, based on 13C measurements. In both planophiles and erectophiles, shaded leaves had greater leaf absorptivity and lower activities of key C4 enzymes than sun leaves. The erectophile form is considered more productive because it allows a more effective distribution of light through the canopy to support photosynthesis. We show that in sorghum, it provides a second benefit, maintenance of higher ΦCO2,max,app to support efficient use of that light resource.

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

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.

Diverse Mechanisms Regulate the Expression of Genes Coding for C4 Enzymes

Most of the enzymes of the C4 pathway of photosynthesis are compartmentalised in either mesophyll or bundle sheath cells. We have begun to dissect the mechanisms controlling the cell-specific expression of genes coding for C4 enzymes by locating the regulatory DNA sequences from two genes in the transformable C4 dicot, Flaveria bidentis. We show that chloroplast and cytosolic forms of pyruvate,orthophosphate dikinase are encoded by a single gene, Pdk. By fusing selected regions of the Pdk gene, to the gusA reporter gene we were able to infer promoter activities from measurements of GUS enzyme activity in transgenic F. bidentis plants. We show that the 5´ end of the Pdk gene contains sequences controlling high-level, mesophyll-specific expression of the C4 form of the enzyme. The promoter controlling low-level expression of the cytosolic form was located in the large intron. The C4 isoform of NADP-malic enzyme is encoded by the Me1 gene. Analyses of a series of reporter gene fusions showed that sequences at the 5´ end of the gene control bundle sheath expression but that sequences located near the 3´ end are necessary for high-level expression. The mechanisms regulating the expression of both genes are clearly different and suggest that there is no universal mechanism controlling the expression of genes coding for C4 enzymes.