The photosynthetic capacity of leaves is determined by their content of nitrogen (N). Nitrogen involved in photosynthesis is divided between soluble proteins and thylakoid membrane proteins. In C4 plants, the photosynthetic apparatus is partitioned between two cell types: mesophyll cells and bundle sheath. The enzymes involved in the C4 carbon cycle and assimilation of nitrogen are localized in a cell-specific manner. Although intracellular distribution of enzymes of N and carbon assimilation is variable, little is known about the physiological consequences of this distribution caused by light changes. Light intensity and nitrogen concentration influence content of nitrates in leaves and can induce activity of the main enzymes involved in N metabolism, and changes that reduce the photosynthesis rate also reduce photosynthetic N use efficiency. In this review, we wish to highlight and discuss how/whether light intensity can improve photosynthesis in maize during nitrogen limitation. We described the general regulation of changes in the main photosynthetic and nitrogen metabolism enzymes, their quantity and localization, thylakoid protein abundance, intracellular transport of organic acids as well as specific features connected with C4 photosynthesis, and addressed the major open questions related to N metabolism and effects of light on photosynthesis in C4 plants.

We investigated the organization of photosystem II (PSII) in agranal bundle sheath thylakoids from a C₄ plant maize. Using blue native/SDS-PAGE and single particle analysis, we show for the first time that PSII in the bundle sheath (BS) chloroplasts exists in a dimeric form and forms light-harvesting complex II (LHCII)·PSII supercomplexes. We also demonstrate that a similar set of photosynthetic membrane complexes exists in mesophyll and agranal BS chloroplasts, including intact LHCI·PSI supercomplexes, PSI monomers, PSII core dimers, PSII monomers devoid of CP43, LHCII trimers, LHCII monomers, ATP synthase, and cytochrome b₆f complex. Fluorescence functional measurements clearly indicate that BS chloroplasts contain PSII complexes that are capable of performing charge separation and are efficiently sensitized by the associated LHCII. We identified a fraction of LHCII present within BS thylakoids that is weakly energetically coupled to the PSII reaction center; however, the majority of BS LHCII is shown to be tightly connected to PSII. Overall, we demonstrate that organization of the photosynthetic apparatus in BS agranal chloroplasts of a model C₄ plant is clearly distinct from that of the stroma lamellae of the C₃ plants. In particular, supramolecular organization of the dimeric LHCII·PSII in the BS thylakoids strongly suggests that PSII in the BS agranal membranes may donate electrons to PSI. We propose that the residual PSII activity may supply electrons to poise cyclic electron flow around PSI and prevent PSI overoxidation, which is essential for the CO₂ fixation in BS cells, and hence, may optimize ATP production within this compartment.