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Nutrient-driven TOR signaling mediates transcriptional repression by promoting translation to regulate plant growth [RNA-seq]

ABSTRACT: As is well known, nutrition is essential for plant growth and development. Extensive research has demonstrated that the target of rapamycin (TOR) is a crucial growth regulator, receiving nutritional inputs in eukaryotic cells. Nevertheless, the precise mechanisms by which TOR coordinates nutrient conditions and growth remain elusive in plants. In this study, we identified a novel transcriptional repression complex, TRCG, downstream of the TOR signaling pathway. This complex is responsible for regulating plant growth and the nutritional response. In the presence of favorable nutritional conditions, TOR is activated, leading to the translation of the 5’-terminal oligopyrimidine (5’-TOP) mRNA of TRCG. TRCG directly binds numerous nutrition-responsive genes, particularly those belonging to the ERF family of transcription factors, to repress their transcription. This repression is achieved by influencing the initiation and elongation of RNA polymerase II (Pol II), thereby maintaining growth and development. In the absence of nutritional conditions, TOR activity is inhibited, resulting in the repression of TRCG translation. This, in turn, relieves the repression of nutrient response genes, causing a stagnation of growth and poor nutrient resistance, thus contributing to the survival of the plant. Moreover, we observed a higher histone H3 and H4K5 acetylation level in the TRCG targets. Acetylated chromatin has long been associated with transcriptional activation, suggesting that TRCG could bind to acetylated chromatin to repress transcriptional activation. Our findings elucidate a previously unidentified precise mechanism by which TOR-mediated transcriptional repression occurs through the stimulation of translation, thereby regulating plant growth and the nutritional response.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE276446 | GEO | 2025/08/11

REPOSITORIES: GEO

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Project description:The nutritional environments that organisms experience are inherently variable, requiring tight coordination of how resources are allocated to different functions relative to the total amount of resources available. A growing body of evidence supports the hypothesis that key endocrine pathways play a fundamental role in this coordination. In particular, the insulin/insulin-like growth factor signaling (IIS) and target of rapamycin (TOR) pathways have been implicated in nutrition-dependent changes in metabolism and nutrient allocation, however little is known about the genetic basis of standing variation in the pathways. To characterize natural genetic variation in the IIS/TOR pathway, we used over 250 recombinant inbred lines (RILs) derived from a multiparental mapping population, the Drosophila Synthetic Population Resource (DSPR), to map QTL for transcript levels of the genes encoding 52 of the core components of the IIS/TOR pathway in three different nutritional environments (dietary restriction, control, and high sugar). In addition, we assayed lifespan for 80 RILs in both dietary restriction and control diets. We identified cis (i.e., local) QTL for six transcripts, all of which are significant in multiple nutrient environments. Further, we identified trans (i.e., distant) QTL for two transcripts, specific to a single nutrient environment, and one “plasticity” QTL that influences the change in gene expression between the control and high sugar diet. Nearly all transcripts, 85%, were significantly differentially expressed between diets. A discriminant function analysis for the control and dietary restriction treatments identified which transcripts best predict the diet treatment. The resulting composite discriminant function scores are correlated with median lifespan (r = 0.45) and mapping these scores revealed a significant QTL within the dietary restriction diet. Our results corroborate the association between the IIS/TOR pathway and the increase in lifespan under dietary restriction in a natural population and identify new locations in the genome involved in regulating the IIS/TOR pathway.

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Nutrient-driven TOR signaling mediates transcriptional repression by promoting translation to regulate plant growth [RNA-seq]

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