Autophagic pathway contributes to low-nitrogen tolerance by optimizing nitrogen uptake and utilization in tomato

Abstract

Autophagy is a primary process involved in the degradation and reuse of redundant or damaged cytoplasmic components in eukaryotes. Autophagy has been demonstrated to facilitate nutrient recycling and remobilization by delivering intracellular materials to the vacuole for degradation in plants under nutrient starvation. However, the role of autophagy in nitrogen (N) uptake and utilization remains unknown. Here, we report that the ATG6-dependent autophagic pathway regulates N utilization in tomato (<i>Solanum lycopersicum</i>) under low-nitrogen (LN) conditions. Autophagy-disrupted mutants exhibited weakened biomass production and N accumulation compared with wild-type (WT), while <i>ATG6</i> overexpression promoted autophagy and biomass production under LN stress. The N content in <i>atg6</i> mutants decreased while that in <i>ATG6</i>-overexpressing lines increased due to the control of N transporter gene expression in roots under LN conditions. Furthermore, ATG6<i>-</i>dependent autophagy enhanced N assimilation efficiency and protein production in leaves. Nitrate reductase and nitrite reductase activities and expression were compromised in <i>atg6</i> mutants but were enhanced in <i>ATG6</i>-overexpressing plants under LN stress. Moreover, ATG6-dependent autophagy increased plant carbon fixation and photosynthetic capacity. The quantum yield of photosystem II, photosynthetic N use efficiency and photosynthetic protein accumulation were compromised in <i>atg6</i> mutants but were restored in <i>ATG6</i>-overexpressing plants. A WT scion grafted onto <i>atg6</i> mutant rootstock and an <i>atg6</i> scion grafted onto WT rootstock both exhibited inhibited LN-induced autophagy and N uptake and utilization. Thus, ATG6-dependent autophagy regulates not only N uptake and utilization as well as carbon assimilation but also nutrient recycling and remobilization in tomato plants experiencing LN stress.