TOR (target of rapamycin) is a key regulator of triacylglycerol accumulation in microalgae

Imamura, Sousuke; Kawase, Yasuko; Kobayashi, Ikki; Shimojima, Mie; Ohta, Hiroyuki; Tanaka, Kan

doi:10.1080/15592324.2016.1149285

Cited by 50 publications

(48 citation statements)

References 13 publications

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“…To gain insight on the effect of TOR kinase inhibition at the cellular level, we carried out a detailed microscopic study of C. reinhardtii cells treated with AZD8055 for 2, 4, 8, and 12 hr of treatment. As has been reported earlier for TOR kinase inhibition by rapamycin and AZD8055 (Imamura et al, ; Pérez‐Pérez & Crespo, ), we also observed a gradual increase in the size of cells upon AZD treatment for 2, 4, 8, and 12 hr. Lipid accumulation also increased upon 12 hr of AZD treatment (Figure a) as previously reported (Imamura et al, ).…”

Section: Resultssupporting

confidence: 90%

“…As has been reported earlier for TOR kinase inhibition by rapamycin and AZD8055 (Imamura et al, ; Pérez‐Pérez & Crespo, ), we also observed a gradual increase in the size of cells upon AZD treatment for 2, 4, 8, and 12 hr. Lipid accumulation also increased upon 12 hr of AZD treatment (Figure a) as previously reported (Imamura et al, ). Interestingly, the cup‐shaped structure of the chloroplast is essentially lost by 12 hr AZD and rapamycin treatment (Figure a; Figure a,b).…”

Section: Resultssupporting

confidence: 90%

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Reciprocal regulation of photosynthesis and mitochondrial respiration by TOR kinase in Chlamydomonas reinhardtii

Upadhyaya

Rao

2019

Plant Direct

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While the role of TOR kinase in the chloroplast biogenesis and transcriptional regulation of photosynthesis is well documented in Arabidopsis, the functional relevance of this metabolic sensor kinase in chloroplast–mitochondria cross talk is unknown. Using Chlamydomonas reinhardtii as the model system, we demonstrate the role of TOR kinase in the regulation of chloroplast and mitochondrial functions: We show that TOR kinase inhibition impairs the maintenance of high ETR associated with PSII and low NPQ and inhibits efficient state transitions between PSII and PSI. While compromised photosynthetic functions are observed in TOR kinase inhibited cells, same conditions lead to augmentation in mitochondrial basal respiration rate by twofold and concomitantly a rise in ATP production. Interestingly, such upregulated mitochondrial functions in TOR‐inhibited cells are mediated by fragmented mitochondria via upregulating COXIIb and downregulating Hxk1 and AOX1 protein levels. We propose that TOR kinase may act as a sensor that counter‐regulates chloroplast versus mitochondrial functions in a normal C. reinhardtii cell.

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Section: Resultssupporting

confidence: 90%

Section: Resultssupporting

confidence: 90%

Reciprocal regulation of photosynthesis and mitochondrial respiration by TOR kinase in Chlamydomonas reinhardtii

Upadhyaya

Rao

2019

Plant Direct

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“…Accordingly, a number of studies have shown that TOR inhibition in Chlamydomonas not only globally affects growth and development (Crespo et al ., ), but its function was also shown to negatively control catabolic processes like autophagy (Perez‐Perez et al ., ), while anabolic processes like protein translation were positively controlled by the active TORC1 (Diaz‐Troya et al ., ). Still, even though mounting evidence has accumulated that TOR regulates several metabolic pathways in yeast and mammals (Jewell and Guan, ; Ricoult and Manning, ; Gonzalez and Hall, ), only a few studies have analyzed the impact of TOR inhibition on primary‐ (Lee do and Fiehn, ; Kleessen et al ., ) or lipid‐metabolism (Imamura et al ., , ; Couso et al ., ) in Chlamydomonas. Interestingly, for different reasons all of these studies used unsynchronized batch cultures, which were grown in medium supplemented with acetate as an additional carbon source, precluding physiological and photoautotrophic growth of the green model algae.…”

Section: Introductionmentioning

confidence: 99%

The target of rapamycin kinase affects biomass accumulation and cell cycle progression by altering carbon/nitrogen balance in synchronized Chlamydomonas reinhardtii cells

et al. 2017

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SUMMARYSeveral metabolic processes tightly regulate growth and biomass accumulation. A highly conserved protein complex containing the target of rapamycin (TOR) kinase is known to integrate intra-and extracellular stimuli controlling nutrient allocation and hence cellular growth. Although several functions of TOR have been described in various heterotrophic eukaryotes, our understanding lags far behind in photosynthetic organisms. In the present investigation, we used the model alga Chlamydomonas reinhardtii to conduct a time-resolved analysis of molecular and physiological features throughout the diurnal cycle after TOR inhibition. Detailed examination of the cell cycle phases revealed that growth is not only repressed by 50%, but also that significant, non-linear delays in the progression can be observed. By using metabolomics analysis, we elucidated that the growth repression was mainly driven by differential carbon partitioning between anabolic and catabolic processes. Accordingly, the time-resolved analysis illustrated that metabolic processes including amino acid-, starch-and triacylglycerol synthesis, as well RNA degradation, were redirected within minutes of TOR inhibition. Here especially the high accumulation of nitrogen-containing compounds indicated that an active TOR kinase controls the carbon to nitrogen balance of the cell, which is responsible for biomass accumulation, growth and cell cycle progression.

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“…Recent work reported a connection between TOR kinase and inositol polyphosphate signaling that governs carbon metabolism and lipid accumulation (Couso et al, 2016). Chlamydomonas cells are sensitive to Torin1 and AZD8055 that are potent inhibitors of cell growth at saturating doses (Couso et al, 2016) and induce triacylglycerol accumulation (Imamura et al, 2016). However, the TOR pathway in Chlamydomonas has yet to be characterized extensively and, to date, only a limited number of candidate TOR kinase substrates have been identified.…”

Section: Introductionmentioning

confidence: 99%

Investigating the effect of target of rapamycin kinase inhibition on the Chlamydomonas reinhardtii phosphoproteome: from known homologs to new targets

et al. 2018

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Target of rapamycin (TOR) kinase is a conserved regulator of cell growth whose activity is modulated in response to nutrients, energy and stress. Key proteins involved in the pathway are conserved in the model photosynthetic microalga Chlamydomonas reinhardtii, but the substrates of TOR kinase and downstream signaling network have not been elucidated. Our study provides a new resource for investigating the phosphorylation networks governed by the TOR kinase pathway in Chlamydomonas. We used quantitative phosphoproteomics to investigate the effects of inhibiting Chlamydomonas TOR kinase on dynamic protein phosphorylation. Wild-type and AZD-insensitive Chlamydomonas strains were treated with TOR-specific chemical inhibitors (rapamycin, AZD8055 and Torin1), after which differentially affected phosphosites were identified. Our quantitative phosphoproteomic dataset comprised 2547 unique phosphosites from 1432 different proteins. Inhibition of TOR kinase caused significant quantitative changes in phosphorylation at 258 phosphosites, from 219 unique phosphopeptides. Our results include Chlamydomonas homologs of TOR signaling-related proteins, including a site on RPS6 with a decrease in phosphorylation. Additionally, phosphosites on proteins involved in translation and carotenoid biosynthesis were identified. Follow-up experiments guided by these phosphoproteomic findings in lycopene beta/epsilon cyclase showed that carotenoid levels are affected by TORC1 inhibition and carotenoid production is under TOR control in algae.

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TOR (target of rapamycin) is a key regulator of triacylglycerol accumulation in microalgae

Cited by 50 publications

References 13 publications

Reciprocal regulation of photosynthesis and mitochondrial respiration by TOR kinase in Chlamydomonas reinhardtii

Reciprocal regulation of photosynthesis and mitochondrial respiration by TOR kinase in Chlamydomonas reinhardtii

The target of rapamycin kinase affects biomass accumulation and cell cycle progression by altering carbon/nitrogen balance in synchronized Chlamydomonas reinhardtii cells

Investigating the effect of target of rapamycin kinase inhibition on the Chlamydomonas reinhardtii phosphoproteome: from known homologs to new targets

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