Saccharomyces cerevisiae FKBP12 binds Arabidopsis thaliana TOR and its expression in plants leads to rapamycin susceptibility

Sormani, Rodnay; Yao, Lei; Menand, Benoît; Ennar, Najla; Lecampion, Cécile; Meyer, Christian; Robaglia, Christophe

doi:10.1186/1471-2229-7-26

Cited by 113 publications

(132 citation statements)

References 38 publications

Supporting

Mentioning

121

Contrasting

Unclassified

Order By: Relevance

“…The severity of these phenotypes increased with increasing concentrations of rapamycin, with even a dose of 0.5 µg/mL rapamycin being sufficient to observe effects on seedling growth in all the four BP12 lines ( Figure 1D). These results clearly indicate that Arabidopsis seedling growth and the observed root and shoot phenotypes are dependent on both the FKBP12 transgene expression and rapamycin, consistent with previous observations (Mahfouz et al, 2006;Sormani et al, 2007;Leiber et al, 2010). We would like to note here that compared with the findings with transgenic Arabidopsis lines, the wild-type seedling growth was normal even at the highest concentration of rapamycin tested (i.e., 20 µg/mL medium) ( Figure 1D).…”

supporting

confidence: 80%

“…Rapamycin specifically binds to FKBP12 (for FK506 binding protein 12), which interacts with the FRB domain of TOR, and the resultant rapamycin-FKBP12-TOR inhibitory complex renders the TOR pathway inactive (Heitman et al, 1991;Stan et al, 1994;Zheng et al, 1995;Loewith et al, 2002). Studies with Arabidopsis have shown that rapamycin treatment does not produce phenotypes associated with inhibition of TOR, and this is attributed to structural differences of the target Arabidopsis FKBP12 proteins, which are unlike their yeast or mammalian counterparts (Xu et al, 1998;Menand et al, 2002;Sormani et al, 2007). This is further supported by studies that showed that transgenic Arabidopsis plants that expressed yeast or human FKBP12 proteins are rapamycin sensitive Leiber et al, 2010;Xiong and Sheen, 2012).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

et al. 2012

View full text Add to dashboard Cite

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 ...

show abstract

supporting

confidence: 80%

Section: Introductionmentioning

confidence: 99%

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

et al. 2012

View full text Add to dashboard Cite

show abstract

“…However, the FKBP12 gene does render TOR sensitive to rapamycin, as long as FKBP12 is expressed at a sufficient level (Xiong and Sheen, 2012). Cereals are also sensitive to the drug (Agredano-Moreno et al, 2007;Schepetilnikov et al, 2011), and Arabidopsis TOR becomes more sensitive to rapamycin when a human or yeast FK506 binding protein is expressed in Arabidopsis (Mahfouz et al, 2006;Sormani et al, 2007;Ren et al, 2012). Arabidopsis TOR is also sensitive to the novel mammalian TOR inhibitor, Torin1 (Schepetilnikov et al, 2013).…”

Section: Tor Kinasementioning

confidence: 99%

Translational Regulation of Cytoplasmic mRNAs

Roy

Arnim

2013

The Arabidopsis Book

View full text Add to dashboard Cite

Translation of the coding potential of a messenger RNA into a protein molecule is a fundamental process in all living cells and consumes a large fraction of metabolites and energy resources in growing cells. Moreover, translation has emerged as an important control point in the regulation of gene expression. At the level of gene regulation, translational control is utilized to support the specific life histories of plants, in particular their responses to the abiotic environment and to metabolites. This review summarizes the diversity of translational control mechanisms in the plant cytoplasm, focusing on specific cases where mechanisms of translational control have evolved to complement or eclipse other levels of gene regulation. We begin by introducing essential features of the translation apparatus. We summarize early evidence for translational control from the pre-Arabidopsis era. Next, we review evidence for translation control in response to stress, to metabolites, and in development. The following section emphasizes RNA sequence elements and biochemical processes that regulate translation. We close with a chapter on the role of signaling pathways that impinge on translation.

show abstract

“…Arabidopsis TOR displays a weak sensitivity to the peptidyl-prolyl cis/trans isomerase (FK506-binding protein 12 [FKBP12])-rapamycin complex (Menand et al, 2002;Sormani et al, 2007), or becomes sensitive when human or yeast FKBP12 is overexpressed in Arabidopsis or high rapamycin concentrations are applied to inhibit growth (Mahfouz et al, 2006;Sormani et al, 2007;Ren et al, 2012;Xiong and Sheen, 2012). Currently, ATP-competitive inhibitors such as Torin-1 and the second-generation inhibitor AZD-8055 are used widely to block TOR in plants (Montané and Menand, 2013;Schepetilnikov et al, 2013Schepetilnikov et al, , 2017.…”

Section: Plant Tor Complex Compositionmentioning

confidence: 99%

Recent Discoveries on the Role of TOR (Target of Rapamycin) Signaling in Translation in Plants

2017

View full text Add to dashboard Cite

Protein synthesis is an intricate, energy-demanding, and tightly controlled process that plays a fundamental role in cell growth, proliferation, and differentiation. The target of rapamycin (TOR) protein kinase integrates stress-, nutrient-, and energy-related signals to optimize protein synthesis outputs. In mammals, TOR is a main controller of capped mRNA translation; how TOR participates in translation initiation in plants is unclear, but active TOR is required for regulation of translation of mRNA with 59-untranslated region (59-UTR) upstream open reading frames (uORFs)-known translation regulatory elements in eukaryotes. Recent data implicates diverse signals such as stress, hormones, and metabolites in regulation of TOR signal transduction pathways and, thus, in response to environmental stress. Here, we review current knowledge of plant TOR complex composition and activation, and its function in translation, compiling data on downstream processes that are under stringent control of TOR in mammals but not yet investigated in plants.Plants have evolved various adaptation mechanisms to ensure their optimal growth, with plant development and behavior being strongly responsive to various external and internal stimuli. By monitoring their environment, plants trigger signal transduction cascades in order to regulate downstream cellular processes, mainly via protein synthesis-a major energy-consuming process (Buttgereit and Brand, 1995). The TOR protein kinase integrates extracellular signals (hormones, biotic and abiotic stresses, growth factors) together with intracellular nutrient availability and energy status to control protein synthesis and other anabolic processes if conditions are favorable, and represses catabolic processes such as autophagy (Albert and Hall, 2015). The past 10 years has boosted research on plant TOR complex composition, highlighted TOR upstream signals and downstream targets, and revealed an interplay between TOR signaling and hormonal, stress, and other pathways in photosynthetic organisms. We are beginning to understand how TOR is activated, and how it controls many cellular processes, such as transcription, translation, and autophagy. Here, we give an overview of recent results on the role of TOR in plant translation control and draw the reader's attention to future questions to address. In plants, inactivation of TOR correlates with a decrease in total polysomal levels (Deprost et al., 2007;Schepetilnikov et al., 2011Schepetilnikov et al., , 2013, strongly suggesting a role for TOR in plant translation. Although a role for TOR in global translation in plants has been documented, the players and mechanisms used to influence different steps of translation initiation -the step most controlled by TOR in mammals-are only starting to emerge. Here, we summarize the current state of knowledge of specific plant translation initiation mechanisms that are controlled by 59-UTR elements of mRNAs and discuss regulation of these mechanisms by TOR/S6 kinase 1 (S6K1) signaling. Examples where TOR re...

show abstract

Saccharomyces cerevisiae FKBP12 binds Arabidopsis thaliana TOR and its expression in plants leads to rapamycin susceptibility

Cited by 113 publications

References 38 publications

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

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

Translational Regulation of Cytoplasmic mRNAs

Recent Discoveries on the Role of TOR (Target of Rapamycin) Signaling in Translation in Plants

Contact Info

Product

Resources

About