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Article|02 Dec 2022|OPEN
Theanine, a tea-plant-specific non-proteinogenic amino acid, is involved in the regulation of lateral root development in response to nitrogen status
Tingting Chen1 ,† , Shijia Lin1 ,† , Ziping Chen1 ,† , Tianyuan Yang1 , Shupei Zhang1 , Jinsong Zhang1 , Guohua Xu2 , Xiaochun Wan1 and Zhaoliang Zhang,1 ,
1State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei 230036, China
2State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing 210095, China
*Corresponding author. E-mail: zhlzhang@ahau.edu.cn
Tingting Chen,Shijia Lin and Ziping Chen contributed equally to the study.

Horticulture Research 10,
Article number: uhac267 (2023)
doi: https://doi.org/10.1093/hr/uhac267
Views: 303

Received: 21 Sep 2022
Accepted: 28 Nov 2022
Published online: 02 Dec 2022

Abstract

Glutamine synthetase type I (GSI)-like proteins are proposed to mediate nitrogen signaling and developmental fate by synthesizing yet unidentified metabolites. Theanine, the most abundant non-proteinogenic amino acid in tea plants, is the first identified metabolite synthesized by a GSI-like protein (CsTSI) in a living system. However, the roles of theanine in nitrogen signaling and development are little understood. In this study we found that nitrogen deficiency significantly reduced theanine accumulation and increased lateral root development in tea plant seedlings. Exogenous theanine feeding significantly repressed lateral root development of seedlings of tea plants and the model plant Arabidopsis. The transcriptomic analysis revealed that the differentially expressed genes in the roots under theanine feeding were enriched in the apoplastic pathway and H2O2 metabolism. Consistently, theanine feeding reduced H2O2 levels in the roots. Importantly, when co-treated with H2O2, theanine abolished the promoting effect of H2O2 on lateral root development in both tea plant and Arabidopsis seedlings. The results of histochemical assays confirmed that theanine inhibited reactive oxygen species accumulation in the roots. Further transcriptomic analyses suggested the expression of genes encoding enzymes involved in H2O2 generation and scavenging was down- and upregulated by theanine, respectively. Moreover, the expression of genes involved in auxin metabolism and signaling, cell division, and cell expansion was also regulated by theanine. Collectively, these results suggested that CsTSI-synthesized theanine is likely involved in the regulation of lateral root development, via modulating H2O2 accumulation, in response to nitrogen levels in tea plants. This study also implied that the module consisting of GSI-like protein and theanine-like metabolite is probably conserved in regulating development in response to nitrogen status in plant species.