Target of Rapamycin Signaling Regulates Metabolism, Growth, and Life Span in Arabidopsis    

Abstract

Target of Rapamycin (TOR) is a major nutrition and energy sensor that regulates growth and life span in yeast and animals. In plants, growth and life span are intertwined not only with nutrient acquisition from the soil and nutrition generation via photosynthesis but also with their unique modes of development and differentiation. How TOR functions in these processes has not yet been determined. To gain further insights, rapamycin-sensitive transgenic Arabidopsis thaliana lines (BP12) expressing yeast FK506 Binding Protein12 were developed. Inhibition of TOR in BP12 plants by rapamycin resulted in slower overall root, leaf, and shoot growth and development leading to poor nutrient uptake and light energy utilization. Experimental limitation of nutrient availability and light energy supply in wild-type Arabidopsis produced phenotypes observed with TOR knockdown plants, indicating a link between TOR signaling and nutrition/light energy status. Genetic and physiological studies together with RNA sequencing and metabolite analysis of TOR-suppressed lines revealed that TOR regulates development and life span in Arabidopsis by restructuring cell growth, carbon and nitrogen metabolism, gene expression, and rRNA and protein synthesis. Gain-and loss-of-function Ribosomal Protein S6 (RPS6) mutants additionally show that TOR function involves RPS6-mediated nutrition and light-dependent growth and life span in Arabidopsis. INTRODUCTIONAmong all extant organisms, many of the longest living species are plants. For example, a creosote bush (Larrea tridentata) called King Clone, which has lived for over 10,000 years, was found in the Mojave Desert (Vasek, 1980). The giant redwood trees in California (Sequoia sempervirens) live for well over 2000 years (Scheres, 2007) and several other tree species have a long life span. However, the mechanisms that underpin longevity in plants are not known. Dissecting the control mechanisms of growth and life span in plants has many implications. It will provide a framework for addressing the key components and regulators of life span in plants. Engineering life span in plants has multiple applications, including early maturation for short seasons, long-lasting horticultural plants, and trees of desirable life span in silviculture (McCouch, 2004;Neale, 2007;Takeda and Matsuoka, 2008;Sonah et al., 2011). Recent work identified genetic factors that can be modified via breeding techniques to improve crop yield through modulating the growth phases (Moose and Mumm, 2008). Uauy et al. (2006) showed that a NAC transcription factor-mediated acceleration of senescence impacted nutrient remobilization in wheat (Triticum aestivum), resulting in significant increase in protein content and micronutrients in the grains (Uauy et al., 2006). Thus, life span alteration can have several beneficial outcomes.Plants are distinct from most other multicellular eukaryotes in having a modular body plan with immortal totipotent stem cells, sessile but autotrophic lifestyle, and very extensive biosynthetic capabilities ...

Transitioning to the Next Phase: The Role of Sugar Signaling throughout the Plant Life Cycle

“…1). In addition to the role of T6P in floral transition, a function of TOR in promoting flowering has been suggested (Ren et al, 2012).…”

Synergism between Inositol Polyphosphates and TOR Kinase Signaling in Nutrient Sensing, Growth Control, and Lipid Metabolism in Chlamydomonas

“…However, the specific downstream signaling targets and intersecting pathways with TOR kinase in plants are still not completely understood, especially as they relate to control of metabolism. Although the Arabidopsis thaliana TOR gene AtTOR is essential (Menand et al, 2002), conditional silencing resulted in early senescence with a decrease in photosynthesis linked to chlorophyll breakdown (Deprost et al, 2007) along with other metabolite changes reflecting altered carbon metabolism (Deprost et al, 2007;Ren et al, 2012;Caldana et al, 2013;Rexin et al, 2015). In Arabidopsis, regulation by sugars is upstream of TOR with glucose activating TOR and promoting cell proliferation in root meristems (Xiong et al, 2013).…”

Inter-subunit interactions between Glutamate-Like Receptors inArabidopsis

“…10 Likewise, Arabidopsis homolog of Target of Rapamycin (TOR) plays a role in integrating nutrition signals including nitrogen in a similar manner as its yeast and animal counterparts. 11 Lastly, the plant homologs of amino acid gated channels from mammals has recently been established as amino acid gated channels, 12,13 representing a potential mechanism for amino acid sensing in plants.…”