Molecular basis of delayed leaf senescence induced by short-term treatment with low phosphate in rice

Leaf senescence is a programmed plant developmental process that can also be regulated by environmental factors, like nutrient availability. Although phosphorus is an essential element determining plants' growth, mechanisms underlying adaptation to phosphorus availability in plants are not well understood. In this study, we combined physiological, biochemical and molecular approaches to investigate the effect of phosphate supply on leaf senescence in rice, one of the world's most important crops. We show that short-term treatment of rice seedlings with low phosphate increases photosynthetic pigments content, confers tolerance to methyl viologen-induced oxidative stress in chloroplasts, and increases antioxidant enzyme activities. Low-phosphate-treated plants also showed a reduction in membrane lipid peroxidation and electrolyte leakage in leaves. Opposite trends were observed in seedlings under high phosphate supply, in which accelerated leaf senescence occurs. Further, CRISPR/Cas9-mediated editing of MIR827, and subsequent reduction in Pi content, delays leaf senescence, while MIR827 and MIR399 overexpression causes Pi accumulation and promotes leaf senescence. Thus, miR399 and miR827 play a role in regulating leaf senescence in rice, likely through modulation of cellular Pi homeostasis. Transcriptomic analysis of low phosphate-treated plants demonstrated a coordinated regulation of multiple biological processes related not only to the biosynthesis of photosynthetic pigments and senescence-associated processes, but also in diverse metabolic processes. These findings support delayed leaf senescence in response to low phosphate supply in rice, while illustrating the diversity of regulatory networks governing leaf senescence. Unravelling processes controlling adaptation to low phosphate supply during the rice vegetative stage will help in optimizing phosphorus fertilizer application in rice fields.