Comparative transcriptomics reveals the role of altered energy metabolism in the establishment of single-cell C(4) photosynthesis in Bienertia sinuspersici

Single-cell C(4) photosynthesis (SCC(4)) in terrestrial plants without Kranz anatomy involves three steps: initial CO(2) fixation in the cytosol, CO(2) release in mitochondria, and a second CO(2) fixation in central chloroplasts. Here, we investigated how the large number of mechanisms underlying these processes, which occur in three different compartments, are orchestrated in a coordinated manner to establish the C(4) pathway in Bienertia sinuspersici, a SCC(4) plant. Leaves were subjected to transcriptome analysis at three different developmental stages. Functional enrichment analysis revealed that SCC(4) cycle genes are coexpressed with genes regulating cyclic electron flow and amino/organic acid metabolism, two key processes required for the production of energy molecules in C(3) plants. Comparative gene expression profiling of B. sinuspersici and three other species (Suaeda aralocaspica, Amaranthus hypochondriacus, and Arabidopsis thaliana) showed that the direction of metabolic flux was determined via an alteration in energy supply in peripheral chloroplasts and mitochondria via regulation of gene expression in the direction of the C(4) cycle. Based on these results, we propose that the redox homeostasis of energy molecules via energy metabolism regulation is key to the establishment of the SCC(4) pathway in B. sinuspersici.