Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice

BMC Plant Biol. 2020 Apr 7;20(1):143. doi: 10.1186/s12870-020-02363-x.

Abstract

Background: Overuse of nitrogen fertilizers is often a major practice to ensure sufficient nitrogen demand of high-yielding rice, leading to persistent NH4+ excess in the plant. However, this excessive portion of nitrogen nutrient does not correspond to further increase in grain yields. For finding out the main constraints related to this phenomenon, the performance of NH4+ excess in rice plant needs to be clearly addressed beyond the well-defined root growth adjustment. The present work isolates an acute NH4+ excess condition in rice plant from causing any measurable growth change and analyses the initial performance of such internal NH4+ excess.

Results: We demonstrate that the acute internal NH4+ excess in rice plant accompanies readily with a burst of reactive oxygen species (ROS) and initiates the downstream reactions. At the headstream of carbon production, photon caption genes and the activity of primary CO2 fixation enzymes (Rubisco) are evidently suppressed, indicating a reduction in photosynthetic carbon income. Next, the vigorous induction of glutathione transferase (GST) genes and enzyme activities along with the rise of glutathione (GSH) production suggest the activation of GSH cycling for ROS cleavage. Third, as indicated by strong induction of glycolysis / glycogen breakdown related genes in shoots, carbohydrate metabolisms are redirected to enhance the production of energy and carbon skeletons for the cost of ROS scavenging. As the result of the development of these defensive reactions, a carbon scarcity would accumulatively occur and lead to a growth inhibition. Finally, a sucrose feeding cancels the ROS burst, restores the activity of Rubisco and alleviates the demand for the activation of GSH cycling.

Conclusion: Our results demonstrate that acute NH4+ excess accompanies with a spontaneous ROS burst and causes carbon scarcity in rice plant. Therefore, under overuse of N fertilizers carbon scarcity is probably a major constraint in rice plant that limits the performance of nitrogen.

Keywords: Carbon scarcity; GSH cycle; NH4+ excess; ROS; Rice; Sucrose feeding.

MeSH terms

  • Ammonium Compounds / adverse effects
  • Ammonium Compounds / metabolism*
  • Fertilizers / adverse effects*
  • Gene Expression Regulation, Plant
  • Glutathione / metabolism
  • Oryza / genetics
  • Oryza / metabolism*
  • Photosynthesis*
  • Reactive Oxygen Species / metabolism*

Substances

  • Ammonium Compounds
  • Fertilizers
  • Reactive Oxygen Species
  • Glutathione