Abstract
The role of pyrophosphate in primary metabolism is poorly understood. Here, we report on the transient down-regulation of plastid-targeted soluble inorganic pyrophosphatase in Nicotiana benthamiana source leaves. Physiological and metabolic perturbations were particularly evident in chloroplastic central metabolism, which is reliant on fast and efficient pyrophosphate dissipation. Plants lacking plastidial soluble inorganic pyrophosphatase (psPPase) were characterized by increased pyrophosphate levels, decreased starch content, and alterations in chlorophyll and carotenoid biosynthesis, while constituents like amino acids (except for histidine, serine, and tryptophan) and soluble sugars and organic acids (except for malate and citrate) remained invariable from the control. Furthermore, translation of Rubisco was significantly affected, as observed for the amounts of the respective subunits as well as total soluble protein content. These changes were concurrent with the fact that plants with reduced psPPase were unable to assimilate carbon to the same extent as the controls. Furthermore, plants with lowered psPPase exposed to mild drought stress showed a moderate wilting phenotype and reduced vitality, which could be correlated to reduced abscisic acid levels limiting stomatal closure. Taken together, the results suggest that plastidial pyrophosphate dissipation through psPPase is indispensable for vital plant processes.
Highlights
The role of pyrophosphate in primary metabolism is poorly understood
We demonstrate that a transient repression of the native plastidial soluble inorganic pyrophosphatase (psPPase) gene using virus-induced gene silencing (VIGS) led to increased PPi levels associated with altered starch, chlorophyll, carotenoid, malate, and His contents as well as affected photosynthesis in Nicotiana benthamiana leaves
Reduced psPPase led to plants that were less able to cope with drought stress due to an inability to synthesize sufficient abscisic acid (ABA), which leads to an inefficiency to promote stomatal closure
Summary
The role of pyrophosphate in primary metabolism is poorly understood. Here, we report on the transient down-regulation of plastid-targeted soluble inorganic pyrophosphatase in Nicotiana benthamiana source leaves. Translation of Rubisco was significantly affected, as observed for the amounts of the respective subunits as well as total soluble protein content These changes were concurrent with the fact that plants with reduced psPPase were unable to assimilate carbon to the same extent as the controls. We demonstrate that a transient repression of the native psPPase gene using virus-induced gene silencing (VIGS) led to increased PPi levels associated with altered starch, chlorophyll, carotenoid, malate, and His contents as well as affected photosynthesis in Nicotiana benthamiana leaves. The results presented here suggest that psPPase is essential for the removal of PPi, which plays a central role in basic cellular function and maintenance, with little or no metabolic compensation by other plastidial PPi-removal mechanisms, demonstrating the importance of this enzyme for maintaining plastidial PPi concentrations at low steady-state levels
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