Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/5/2012
Publication Date: 12/28/2012
Citation: Ren, M., Venglat, P., Qiu, S., Feng, L., Cao, Y., Wang, E., Xiang, D., Wang, J., Alexander, D., Chalivendra, S., Logan, D., Mattoo, A.K., Selvaraj, G., Datla, R. 2012. Target of rapamycin signaling regulates metabolism, growth, and lifespan in Arabidopsis. The Plant Cell. 24:4850-4874. Interpretive Summary: Understanding processes that regulate lifespan of plants and plant organs is fundamental to longevity and has many benefits including long lasting horticultural plants including extended postharvest life of fruits, early maturing crops during short seasons and improving crop yields in general. Studies on animals and yeast have unearthed a relationship between sensors of nutrient and energy use with lifespan through a signaling pathway called TOR (target of rapamycin). In plants, limited information is available on TOR and factors that control post-embryonic growth and lifespan. In a collaborative research between scientists in Canada, USA and France with the USDA-ARS scientist, TOR signaling was found associated with growth and lifespan of the model plant Arabidopsis. Global gene expression and metabolite profiles associated with plant TOR signaling network were identified and quantified. Along with TOR, another member in the network was identified as ribosomal protein S6 (RPS6). This manuscript provides extensive and compelling evidence that TOR and RPS6 work in concert to impact growth, flowering time, and senescence in plants. From these studies it is also conceivable that TOR and its signaling network could be modulated in future studies to engineer plants with the ability to make them resilient against extreme environments. This research is of major interest to plant biologists, horticulturists, agronomists, breeders and geneticist.
Technical Abstract: TOR is a major nutrition and energy sensor that regulates growth and lifespan in yeast and animals. In plants growth and lifespan are intertwined with not only nutrient acquisition but also nutrition generation and unique aspects of development and differentiation. How TOR functions in these processes has remained an open question thus far. To address this, we took a genetic approach by developing rapamycin-sensitive transgenic BP12 Arabidopsis lines. Inhibition of TOR in BP12 plants reduced cell expansion suppressing overall root and leaf development that resulted in poor nutrient uptake and light energy utilization. Limiting nutrient and light energy supply generated phenotypes similar to TOR knockdown in plants, thus linking TOR signaling to nutrition and light energy status. Genetic and physiological analyses together with RNA-Seq and metabolome of TOR-suppressed lines revealed that TOR regulates growth and lifespan in Arabidopsis by restructuring cell growth, metabolism, transcription activity, rRNA and protein synthesis. Using gain- and loss of function RPS6 mutants we further show that TOR function involves RPS6 in determining the nutrition and light dependent growth and lifespan in Arabidopsis with implications to other plant species.