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Article|23 Mar 2022|OPEN
Autophagic pathway contributes to low-nitrogen tolerance by optimizing nitrogen uptake and utilization in tomato
Jiajian Cao1,2 , Xuelian Zheng2 , Dongling Xie2 , Hui Zhou2 and Shujun Shao2,3 , Jie Zhou,2,3 ,
1College of Horticulture, Hunan Agricultural University, Nonda Road 1, Changsha, 410128, China
2Department of Horticulture/Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Yuhangtang Road 866, Hangzhou, 310058, China
3Key Laboratory of Horticultural Plants Growth, Development and Quality Improvement, Agricultural Ministry of China, Yuhangtang Road 866, Hangzhou, 310058, China
*Corresponding author. E-mail: jie@zju.edu.cn

Horticulture Research 9,
Article number: uhac068 (2022)
doi: https://doi.org/10.1093/hr/uhac068
Views: 173

Received: 08 Nov 2021
Accepted: 09 Mar 2022
Published online: 23 Mar 2022

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 (Solanum lycopersicum) under low-nitrogen (LN) conditions. Autophagy-disrupted mutants exhibited weakened biomass production and N accumulation compared with wild-type (WT), while ATG6 overexpression promoted autophagy and biomass production under LN stress. The N content in atg6 mutants decreased while that in ATG6-overexpressing lines increased due to the control of N transporter gene expression in roots under LN conditions. Furthermore, ATG6-dependent autophagy enhanced N assimilation efficiency and protein production in leaves. Nitrate reductase and nitrite reductase activities and expression were compromised in atg6 mutants but were enhanced in ATG6-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 atg6 mutants but were restored in ATG6-overexpressing plants. A WT scion grafted onto atg6 mutant rootstock and an atg6 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.