Targeting TOR signaling for enhanced lipid productivity in algae

Prioretti, Laura; Carrière, Frédéric; Field, Ben; Avilán, Luisana; Montané, Marie‐Hélène; Menand, Benoît; Gontero, Brigitte

doi:10.1016/j.biochi.2019.06.016

Cited by 14 publications

(15 citation statements)

References 83 publications

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“…Another signalling pathway that could play an important role in diatom stress acclimation is the pathway mediated by the nucleotides guanosine tetraphosphate and guanosine pentaphosphate ((p)ppGpp) (Field, 2018; Avilan et al ., 2019; Prioretti et al ., 2020). In bacteria, ppGpp and, to a lesser extent, pppGpp accumulate in response to a range of different stresses, and specifically target transcription and translation to slow growth and promote stress acclimation (Hauryliuk et al ., 2015; Steinchen & Bange, 2016).…”

Section: Introductionmentioning

confidence: 99%

ppGpp influences protein protection, growth and photosynthesis in Phaeodactylum tricornutum

et al. 2021

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Summary Chloroplasts retain elements of a bacterial stress response pathway that is mediated by the signalling nucleotides guanosine penta‐ and tetraphosphate ((p)ppGpp). In the model flowering plant Arabidopsis, ppGpp acts as a potent regulator of plastid gene expression and influences photosynthesis, plant growth and development. However, little is known about ppGpp metabolism or its evolution in other photosynthetic eukaryotes. Here, we studied the function of ppGpp in the diatom Phaeodactylum tricornutum using transgenic lines containing an inducible system for ppGpp accumulation. We used these lines to investigate the effects of ppGpp on growth, photosynthesis, lipid metabolism and protein expression. We demonstrate that ppGpp accumulation reduces photosynthetic capacity and promotes a quiescent‐like state with reduced proliferation and ageing. Strikingly, using nontargeted proteomics, we discovered that ppGpp accumulation also leads to the coordinated upregulation of a protein protection response in multiple cellular compartments. Our findings highlight the importance of ppGpp as a fundamental regulator of chloroplast function across different domains of life, and lead to new questions about the molecular mechanisms and roles of (p)ppGpp signalling in photosynthetic eukaryotes.

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Section: Introductionmentioning

confidence: 99%

ppGpp influences protein protection, growth and photosynthesis in Phaeodactylum tricornutum

et al. 2021

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“…Like plants, diatoms possess signalling pathways with prokaryotic origins such as the bacterial histidine-kinase-based two-component systems (Bowler et al , 2008), as well as pathways of eukaryotic origins such as the Target Of Rapamycin (TOR) kinase (Prioretti et al , 2017; Prioretti et al , 2019) and the G protein-coupled receptor signalling pathway (Port et al 2013).…”

Section: Introductionmentioning

confidence: 99%

ppGpp influences protein protection, growth and photosynthesis inPhaeodactylum tricornutum

Avilán

Lebrun

Puppo

et al. 2020

Preprint

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Chloroplasts retain elements of a bacterial stress response pathway that is mediated by the signalling nucleotides guanosine penta-and tetraphosphate, or (p)ppGpp. In the model flowering plant Arabidopsis, ppGpp acts as a potent regulator of plastid gene expression and influences photosynthesis, plant growth and development.However, little is known about ppGpp metabolism or its evolution in other photosynthetic eukaryotes.• Here, we studied the function of ppGpp in the diatom P. tricornutum using transgenic lines containing an inducible system for ppGpp accumulation. We used these lines to investigate the effects of ppGpp on growth, photosynthesis, lipid metabolism and protein expression.• We demonstrate that ppGpp accumulation reduces photosynthetic capacity and promotes a quiescent-like state with reduced proliferation and ageing. Strikingly, using non-targeted proteomics, we discovered that ppGpp accumulation also leads to the coordinated upregulation of a protein protection response in multiple cellular compartments.• Our findings highlight the importance of ppGpp as a fundamental regulator of chloroplast function across different domains of life, and lead to new questions about the molecular mechanisms and roles of (p)ppGpp signalling in photosynthetic eukaryotes.

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“…However, a better understanding of the controls of the cell division cycle in response to nutrient shortage and the signaling pathways coupling the cellular growth to energy and lipid homeostasis has the potential to improve the future metabolic engineering strategies of algae. Indeed, emerging evidence suggests that the manipulation of signaling pathways, such as TOR, represents a viable approach to increasing the lipid productivity in algae with little to no growth penalties [35, 268]. Thus, further studies of the signaling networks and the downstream components mediating and linking these biological processes are crucial in bridging a critical knowledge gap, which currently prevents us from achieving the optimal balance between the production of biofuels and biomass in algae employing simple and robust culturing conditions.…”

Section: Discussionmentioning

confidence: 99%

Nitrogen-dependent coordination of cell cycle, quiescence and TAG accumulation in Chlamydomonas

Takeuchi

Benning

2019

Biotechnol Biofuels

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Microalgae hold great promises as sustainable cellular factories for the production of alternative fuels, feeds, and biopharmaceuticals for human health. While the biorefinery approach for fuels along with the coproduction of high-value compounds with industrial, therapeutic, or nutraceutical applications have the potential to make algal biofuels more economically viable, a number of challenges continue to hamper algal production systems at all levels. One such hurdle includes the metabolic trade-off often observed between the increased yields of desired products, such as triacylglycerols (TAG), and the growth of an organism. Initial genetic engineering strategies to improve lipid productivity in microalgae, which focused on overproducing the enzymes involved in fatty acid and TAG biosynthesis or inactivating competing carbon (C) metabolism, have seen some successes albeit at the cost of often greatly reduced biomass. Emergent approaches that aim at modifying the dynamics of entire metabolic pathways by engineering of pertinent transcription factors or signaling networks appear to have successfully achieved a balance between growth and neutral lipid accumulation. However, the biological knowledge of key signaling networks and molecular components linking these two processes is still incomplete in photosynthetic eukaryotes, making it difficult to optimize metabolic engineering strategies for microalgae. Here, we focus on nitrogen (N) starvation of the model green microalga, Chlamydomonas reinhardtii, to present the current understanding of the nutrient-dependent switch between proliferation and quiescence, and the drastic reprogramming of metabolism that results in the storage of C compounds following N starvation. We discuss the potential components mediating the transcriptional repression of cell cycle genes and the establishment of quiescence in Chlamydomonas, and highlight the importance of signaling pathways such as those governed by the target of rapamycin (TOR) and sucrose nonfermenting-related (SnRK) kinases in the coordination of metabolic status with cellular growth. A better understanding of how the cell division cycle is regulated in response to nutrient scarcity and of the signaling pathways linking cellular growth to energy and lipid homeostasis, is essential to improve the prospects of biofuels and biomass production in microalgae.

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Targeting TOR signaling for enhanced lipid productivity in algae

Cited by 14 publications

References 83 publications

ppGpp influences protein protection, growth and photosynthesis in Phaeodactylum tricornutum

ppGpp influences protein protection, growth and photosynthesis in Phaeodactylum tricornutum

ppGpp influences protein protection, growth and photosynthesis inPhaeodactylum tricornutum

Nitrogen-dependent coordination of cell cycle, quiescence and TAG accumulation in Chlamydomonas

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