Target of rapamycin signaling orchestrates growth–defense trade‐offs in plants

Abstract

SummaryPlant defense to microbial pathogens is often accompanied by significant growth inhibition. How plants merge immune system function with normal growth and development is still poorly understood. Here, we investigated the role of target of rapamycin (TOR), an evolutionary conserved serine/threonine kinase, in the plant defense response.We used rice as a model system and applied a combination of chemical, genetic, genomic and cell-based analyses.We demonstrate that ectopic expression of TOR and Raptor (regulatory-associated protein of mTOR), a protein previously demonstrated to interact with TOR in Arabidopsis, positively regulates growth and development in rice. Transcriptome analysis of rice cells treated with the TOR-specific inhibitor rapamycin revealed that TOR not only dictates transcriptional reprogramming of extensive gene sets involved in central and secondary metabolism, cell cycle and transcription, but also suppresses many defense-related genes. TOR overexpression lines displayed increased susceptibility to both bacterial and fungal pathogens, whereas plants with reduced TOR signaling displayed enhanced resistance. Finally, we found that TOR antagonizes the action of the classic defense hormones salicylic acid and jasmonic acid.Together, these results indicate that TOR acts as a molecular switch for the activation of cell proliferation and plant growth at the expense of cellular immunity.

Metabolite Regulatory Interactions Control Plant Respiratory Metabolism via Target of Rapamycin (TOR) Kinase Activation

“…Clearly, other gene targets besides PDH isoforms are involved to account for the observed control of other amino acid respiration (e.g., Ala and Thr) by TOR. In this regard, the general upregulation of amino acid catabolic genes, including PDH1, by inactivation of TOR has been repeatedly observed in previous plant transcriptome analyses (Ren et al, 2012;Xiong et al, 2013;De Vleesschauwer et al, 2018). In addition, disruption of TOR signaling in plants leads to the accumulation of high levels of amino acids and TCA cycle organic acids (Moreau et al, 2012;Ren et al, 2012;Caldana et al, 2013), potentially due to activation of amino acid synthesis (Mubeen et al, 2018).…”

TOR signaling downregulation increases resistance to the cereal killer Fusarium graminearum

“…Previously, it was reported that TOR signaling has a role for the potyvirus infection in Arabidopsis and that the inhibition of TOR activity prevents the disease. 12 10,5 have described that TOR mutants could enhance resistance to different pathogens in Arabidopsis and in rice respectively. Our results are in agreement with both reports, contributing with an extremely important example to the idea that the role of TOR in the plant response to pathogens could be general.…”

Mutation in the Arabidopsis regulatory-associated protein TOR 1B (RAPTOR1B) leads to decreased jasmonates levels in leaf tissue

“…Using rice as a model system (Oryza sativa L. cultivar Kitaake), De Vleesschauwer et al showed that TOR antagonizes the action of JA in leaves. 50 The authors showed that significant upregulation of JA-responsive genes has been detected in TOR and Raptor RNAi plants as well as rapamycin-treated WT, Whereas, TOR overexpression resulted in significant downregulation of JA marker genes as well as significant reduction in the endogenous JA content level relative to WT. 50 Additionally, Raptor RNAi resulted in significant accumulation of JA.…”

“…50 The authors showed that significant upregulation of JA-responsive genes has been detected in TOR and Raptor RNAi plants as well as rapamycin-treated WT, Whereas, TOR overexpression resulted in significant downregulation of JA marker genes as well as significant reduction in the endogenous JA content level relative to WT. 50 Additionally, Raptor RNAi resulted in significant accumulation of JA. 50 This contradicting observation could indicate that there is a functional difference in RAPTOR activity between monocots and dicots.…”