Positional cues for the starch/lipid balance in maize kernels and resource partitioning to the embryo

This study tests the hypotheses that in vivo oxygen levels inside developing maize grains locally affect assimilate partitioning and ATP distribution within the kernel. These questions were addressed through combined topographical analysis (O-2- and ATP-mapping), metabolite profiling, and isotope flux analysis. Internal and external oxygen levels were also experimentally altered. Under ambient conditions, mean O-2 concentration immediately inside starchy endosperm dropped to only 1.4% of atmospheric saturation (approximately 3.8 mu M), but was 10-fold higher in the oil-storing embryo. Increasing the O-2 supply to intact kernels stimulated their O-2 demand, shifted ATP localization within the kernel, and elevated their ATP/ADP ratio. Enhanced O-2 availability also increased steady-state levels of glycolytic intermediates and those of the citric acid cycle, as well as some related pools of free amino acids. Subsequent analyses indicated that starch formation within endosperm, but not lipid biosynthesis within embryo, was adapted to the endogenous low oxygen. Increasing the O-2 supply did not change ADP-glucose levels, activity of ADP-glucose pyrophosphorylase, C-13-labeling of ADP-glucose, or flux of C-14-sucrose into starch. In contrast, enhanced O-2 availability increased C-14-label uptake into the embryo, C-13-labeling of acetyl-coenzyme A, and finally C-14-incorporation into lipids. Lipid accumulation in embryo appeared highest in regions with higher ATP. Consistent with labeling data, a decrease in O-2 supply most strongly affected the embryo, whereas rising O-2 levels expanded ATP-rich zones toward the starch-storing endosperm and the scutellar part of embryo. The latter might be responsible for higher C-14-label uptake into the embryo and flux toward lipid. Collectively, data indicate that the in vivo oxygen distribution in maize kernels markedly affects ATP gradients, metabolite levels, and favors assimilate partitioning toward starch within the O-2-depleted endosperm. Clear advantages are thus evident for peripheral localization of the protein and lipid storing structures in maize kernels.