Abstract

To survive and proliferate in diverse environments with varying climate and nutrient availability, plants modulate their metabolism. Achieving a balance between carbon (C) and nitrogen (N) use such that growth and defense mechanisms can be appropriately controlled is critical for plant fitness. The identification of factors that regulate C/N utilization in plants can make a significant contribution to optimization of plant health. Here we show that pyridox(am)ine 5-phosphate oxidase (PDX3), which regulates vitamin B6 homeostasis, influences C/N balance. The B6 vitamer imbalance resulting from loss of PDX3 leads to over-accumulation of nitrogenous compounds. A combination of increased glutamate dehydrogenase activity, impairment in the photorespiratory cycle and inappropriate use of endogenous ammonium fuel the metabolic imbalance. Growth at elevated CO2 levels further exacerbates the pdx3 phenotypes. Interestingly, serine supplementation rescues growth under high CO2 likely bypassing the phosphorylated pathway of biosynthesis suggesting that this amino acid is an important commodity. We show that PDX3 function appears dispensable upon thermomorphogenesis, a condition that favors C metabolism. Furthermore, while a low ammonium to nitrate ratio likely accounts for overstimulation of salicylic acid (SA) defense responses in pdx3 lines that compromises growth, a basal level of SA protects against loss of PDX3 biochemical function. Overall, the study highlights environmental scenarios where vitamin B6 homeostasis, as managed by the salvage pathway enzyme PDX3, is critical and provides insight into how plants reprogram their metabolism under such conditions.