Mitigating growth-stress tradeoffs via elevated TOR signaling in rice

Abstract

Rice production accounts for approximately half of the freshwater resources utilized in agriculture, resulting in greenhouse gas emissions such as methane (CH4) from flooded paddy fields. To address this challenge, environmentally friendly and cost-effective water-saving techniques have become widely adopted in rice cultivation. However, the implementation of water-saving treatments (WSTs) in paddy-field rice has been associated with a substantial yield loss of up to 50% as well as a reduction in nitrogen use efficiency (NUE). In this study, we discovered that the target of rapamycin (TOR) signaling pathway is compromised in rice under WST. Polysome profiling-coupled transcriptome sequencing (polysome-seq) analysis unveiled a substantial reduction in global translation in response to WST associated with the downregulation of TOR activity. Molecular, biochemical, and genetic analyses revealed new insights into the impact of the positive TOR-S6K-RPS6 and negative TOR-MAF1 modules on translation repression under WST. Intriguingly, ammonium exhibited a greater ability to alleviate growth constraints under WST by enhancing TOR signaling, which simultaneously promoted uptake and utilization of ammonium and nitrogen allocation. We further demonstrated that TOR modulates the ammonium transporter AMT1;1 as well as the amino acid permease APP1 and dipeptide transporter NPF7.3 at the translational level through the 5′ untranslated region. Collectively, these findings reveal that enhancing TOR signaling could mitigate rice yield penalty due to WST by regulating the processes involved in protein synthesis and NUE. Our study will contribute to the breeding of new rice varieties with increased water and fertilizer utilization efficiency.