Low nitrate under waterlogging triggers exodermal suberization to form a barrier to radial oxygen loss in rice roots.

Abstract

To acclimate to hypoxic waterlogged conditions, the roots of wetland plants form a radial oxygen loss (ROL) barrier that can promote oxygen diffusion to the root tips. We hypothesized that the low-nitrate concentrations that occur after molecular oxygen is consumed in waterlogged soils are an environmental trigger for ROL barrier formation in rice (Oryza sativa). We previously identified 128 tissue-specific up/downregulated genes during rice ROL barrier formation. The RiceXPro database showed that many of these genes were differentially regulated in response to nitrogen deficiency. Therefore, we assessed changes in the concentrations of ionic species of nitrogen under stagnant conditions, i.e. in a nutrient solution that mimics waterlogged soil conditions, and examined the effects of an increase or decrease of nitrate in the nutrient solution on ROL barrier formation and exodermal suberization. Preventing nitrate deficiency in the stagnant nutrient solution suppressed the formation of an ROL barrier. Conversely, a decrease in nitrate strongly induced ROL barrier formation, even under aerated conditions. In parallel with ROL barrier formation, suberin lamellae formed at the exodermis. Nitrate deficiency also promoted aerenchyma formation and the enlargement of root diameters. These findings suggest that the severe decline of nitrates under waterlogged conditions is an environmental cue for exodermal suberization to form an ROL barrier in rice roots.