The Interplay between Carbon Availability and Growth in Different Zones of the Growing Maize Leaf

Plants assimilate carbon in their photosynthetic tissues in the light. However, carbon is required during the night and in nonphotosynthetic organs. It is therefore essential that plants manage their carbon resources spatially and temporally and coordinate growth with carbon availability. In growing maize (Zea mays) leaf blades, a defined developmental gradient facilitates analyses in the cell division, elongation, and mature zones. We investigated the responses of the metabolome and transcriptome and polysome loading, as a qualitative proxy for protein synthesis, at dusk, dawn, and 6, 14, and 24 h into an extended night, and tracked whole-leaf elongation over this time course. Starch and sugars are depleted by dawn in the mature zone, but only after an extension of the night in the elongation and division zones. Sucrose (Suc) recovers partially between 14 and 24 h into the extended night in the growth zones, but not the mature zone. The global metabolome and transcriptome track these zone-specific changes in Suc. Leaf elongation and polysome loading in the growth zones also remain high at dawn, decrease between 6 and 14 h into the extended night, and then partially recover, indicating that growth processes are determined by local carbon status. The level of Suc-signaling metabolite trehalose-6-phosphate, and the trehalose-6-phosphate:Suc ratio are much higher in growth than mature zones at dusk and dawn but fall in the extended night. Candidate genes were identified by searching for transcripts that show characteristic temporal response patterns or contrasting responses to carbon starvation in growth and mature zones.