Subdivision of Light Signaling Networks Contributes to Partitioning of C4 Photosynthesis1[OPEN]

Plants coordinate the expression of photosynthesis-related genes in response to growth and environmental changes. In species that conduct two-cell C-4 photosynthesis, expression of photosynthesis genes is partitioned such that leaf mesophyll and bundle sheath cells accumulate different components of the photosynthetic pathway. The identities of the regulatory networks that facilitate this partitioning are unknown. Here, we show that differences in light perception between mesophyll and bundle sheath cells facilitate differential regulation and accumulation of photosynthesis gene transcripts in the C-4 crop maize (Zea mays). Key components of the photosynthesis gene regulatory network differentially accumulated between mesophyll and bundle sheath cells, indicative of differential network activity across cell types. We further show that blue (but not red) light is necessary and sufficient to activate photosystem II assembly in mesophyll cells in etiolated maize. Finally, we demonstrate that 61% of all light-induced mesophyll and bundle sheath genes were induced only by blue light or only by red light, but not both. These findings provide evidence that subdivision of light signaling networks is a component of cellular partitioning of C-4 photosynthesis in maize. Cell-specific activation of photosynthetic machinery is mediated by differences in light signaling networks between photosynthetic cell types; these differences indicate that the regulatory system that facilitates C-4 photosynthesis may have evolved to reinforce differences in within-leaf light availability.