Photosynthetic-Product–Dependent Activation of Plasma Membrane H(+)-ATPase and Nitrate Uptake in Arabidopsis Leaves

Plasma membrane (PM) proton-translocating adenosine triphosphatase (H(+)-ATPase) is a pivotal enzyme for plant growth and development that acts as a primary transporter and is activated by phosphorylation of the penultimate residue, threonine, at the C-terminus. Small Auxin-Up RNA family proteins maintain the phosphorylation level via inhibiting dephosphorylation of the residue by protein phosphatase 2C-D clade. Photosynthetically active radiation activates PM H(+)-ATPase via phosphorylation in mesophyll cells of Arabidopsis thaliana, and phosphorylation of PM H(+)-ATPase depends on photosynthesis and photosynthesis-related sugar supplementation, such as sucrose, fructose and glucose. However, the molecular mechanism and physiological role of photosynthesis-dependent PM H(+)-ATPase activation are still unknown. Analysis using sugar analogs, such as palatinose, turanose and 2-deoxy glucose, revealed that sucrose metabolites and products of glycolysis such as pyruvate induce phosphorylation of PM H(+)-ATPase. Transcriptome analysis showed that the novel isoform of the Small Auxin-Up RNA genes, SAUR30, is upregulated in a light- and sucrose-dependent manner. Time-course analyses of sucrose supplementation showed that the phosphorylation level of PM H(+)-ATPase increased within 10 min, but the expression level of SAUR30 increased later than 10 min. The results suggest that two temporal regulations may participate in the regulation of PM H(+)-ATPase. Interestingly, a (15)NO(3)(−) uptake assay in leaves showed that light increases (15)NO(3)(−) uptake and that increment of (15)NO(3)(−) uptake depends on PM H(+)-ATPase activity. The results opened the possibility of the physiological role of photosynthesis-dependent PM H(+)-ATPase activation in the uptake of NO(3)(−). We speculate that PM H(+)-ATPase may connect photosynthesis and nitrogen metabolism in leaves.