Significance of accumulation of the alarmone (p)ppGpp in chloroplasts for controlling photosynthesis and metabolite balance during nitrogen starvation in Arabidopsis

Honoki, Rina; Ono, Sumire; Oikawa, Akira; Saito, Kazuki; Masuda, Shinji

doi:10.1007/s11120-017-0402-y

Cited by 33 publications

(56 citation statements)

References 41 publications

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“…Indeed, the carbon/nitrogen ratio in AtRSH3oe plants under nitrogen deficiency is significantly lower than in WT plants, suggesting higher nitrogen deficiency tolerance of the mutant plants (Honoki et al 2017). Similarly, in phosphorous-limited conditions, the same line accumulates significantly lower levels of anthocyanins, which is again indicative either of higher nutrient deprivation tolerance or the lack of starvation sensing (Maekawa et al 2015).…”

Section: Role Of Rsh Proteins and Alarmones In Chloroplastsmentioning

confidence: 99%

“…Nitrogen deficiency (p)ppGpp-mediated tolerance occurs also likely due to reduced chlorophyll content, changes in photosynthetic parameters as well as pronounced changes in metabolite levels in AtRSH3oe plants in comparison to WT plants. Thus, it was proposed that (p)ppGpp help plants to function during nitrogen starvation by modulating photosynthetic performance and metabolite balance (Honoki et al 2017). …”

Section: Role Of Rsh Proteins and Alarmones In Chloroplastsmentioning

confidence: 99%

“…Maekawa et al (2015) proposed that the increased plant size might be the effect of metabolite fitness, provoked by decreased photosynthesis. Plants of the AtRSH3oe (in rsh2 rsh3 background) line grow also better in nitrogen starvation conditions, what is likely attributed to changes in photosynthetic activities and metabolite balance (Honoki et al 2017). On the other hand, the results with the AtRSH3oe line (in WT) are supported with the studies on P. patens homologs of AtRSH2 / RSH3 , PpRSH2a and PpRSH2b , as their overexpressor lines show significant growth suppression in a glucose-concentration-dependent manner (Sato et al 2015).…”

Section: Role Of Rsh and Alarmones In Plantsmentioning

confidence: 99%

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Within and beyond the stringent response-RSH and (p)ppGpp in plants

Boniecka

Prusińska

Dąbrowska

et al. 2017

Planta

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Main conclusionPlant RSH proteins are able to synthetize and/or hydrolyze unusual nucleotides called (p)ppGpp or alarmones. These molecules regulate nuclear and chloroplast transcription, chloroplast translation and plant development and stress response.Homologs of bacterial RelA/SpoT proteins, designated RSH, and products of their activity, (p)ppGpp—guanosine tetra—and pentaphosphates, have been found in algae and higher plants. (p)ppGpp were first identified in bacteria as the effectors of the stringent response, a mechanism that orchestrates pleiotropic adaptations to nutritional deprivation and various stress conditions. (p)ppGpp accumulation in bacteria decreases transcription—with exception to genes that help to withstand or overcome current stressful situations, which are upregulated—and translation as well as DNA replication and eventually reduces metabolism and growth but promotes adaptive responses. In plants, RSH are nuclei-encoded and function in chloroplasts, where alarmones are produced and decrease transcription, translation, hormone, lipid and metabolites accumulation and affect photosynthetic efficiency and eventually plant growth and development. During senescence, alarmones coordinate nutrient remobilization and relocation from vegetative tissues into seeds. Despite the high conservancy of RSH protein domains among bacteria and plants as well as the bacterial origin of plant chloroplasts, in plants, unlike in bacteria, (p)ppGpp promote chloroplast DNA replication and division. Next, (p)ppGpp may also perform their functions in cytoplasm, where they would promote plant growth inhibition. Furthermore, (p)ppGpp accumulation also affects nuclear gene expression, i.a., decreases the level of Arabidopsis defense gene transcripts, and promotes plants susceptibility towards Turnip mosaic virus. In this review, we summarize recent findings that show the importance of RSH and (p)ppGpp in plant growth and development, and open an area of research aiming to understand the function of plant RSH in response to stress.

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Section: Role Of Rsh Proteins and Alarmones In Chloroplastsmentioning

confidence: 99%

Section: Role Of Rsh Proteins and Alarmones In Chloroplastsmentioning

confidence: 99%

Section: Role Of Rsh and Alarmones In Plantsmentioning

confidence: 99%

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Within and beyond the stringent response-RSH and (p)ppGpp in plants

Boniecka

Prusińska

Dąbrowska

et al. 2017

Planta

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“…(p)ppGpp is also found in plants and green algae (Takahashi et al , 2004), and chloroplast-localized RelA SpoT Homolog (RSH) enzymes for (p)ppGpp synthesis are widespread among the photosynthetic eukaryotes (Atkinson et al , 2011; Ito et al , 2017; Avilan et al , 2019). Currently, the function of ppGpp is best characterised in the flowering plant Arabidopsis, where it inhibits chloroplast gene expression, reduces chloroplast size, and reduces photosynthetic capacity (Maekawa et al , 2015; Sugliani et al , 2016; Honoki et al , 2018). While the mechanisms are still uncertain, ppGpp may act by downregulating the transcription of chloroplast encoded genes via the inhibition of chloroplastic RNA polymerases or GTP biosynthesis (Nomura et al , 2014; Yamburenko et al , 2015; Sugliani et al , 2016).…”

Section: Introductionmentioning

confidence: 99%

ppGpp influences protein protection, growth and photosynthesis in Phaeodactylum 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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“…The effects of (p)ppGpp on plant growth have been investigated using RSH3-overexpression lines that over-accumulate ppGpp (Maekawa et al 2015;Sugliani et al 2016;Honoki et al 2018). Mutant-specific phenotypes include pale-green leaves, dwarfization of chloroplasts, increased tolerance to nitrogen deficiency, and reduced mRNA levels of chloroplast genes, which indicate that the plastidial stringent response affects plant growth and adaptation to stresses, although the exact targets of (p)ppGpp in chloroplasts are largely unclarified.…”

Section: Introductionmentioning

confidence: 99%

Plastidial (p)ppGpp synthesis by the Ca²⁺-dependent RelA-SpoT homolog regulates the adaptation of chloroplast gene expression to darkness in Arabidopsis

Ono

Suzuki

Ito

et al. 2019

Preprint

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Abbreviations: CRSH, Ca 2+ -activated RSH; flg22, flagellin 22; (p)ppGpp, 5'-di(tri)phosphate 3'-diphosphate; PAMPs; pathogen-associated molecular patterns; RSH, RelA-SpoT homolog; qRT-PCR, quantitative real-time PCR Abstract In bacteria, the hyper-phosphorylated nucleotides, guanosine 5'-diphosphate 3'-diphosphate (ppGpp) and guanosine 5'-triphosphate 3'-diphosphate (pppGpp), function as secondary messengers in the regulation of various metabolic processes of the cell, including transcription, translation, and enzymatic activities, especially under nutrient deficiency. The activity carried out by these nucleotide messengers is known as the stringent response. (p)ppGpp levels are controlled by two distinct enzymes, namely, RelA and SpoT, in Escherichia coli. RelA-SpoT homologs (RSHs) are also conserved in plants and algae where they function in the plastids. The model plant Arabidopsis thaliana contains four RSHs: RSH1, RSH2, RSH3, and Ca 2+ -dependent RSH (CRSH).Genetic characterizations of RSH1, RSH2, and RSH3 were undertaken, which showed that the (p)ppGpp-dependent plastidial stringent response significantly influences plant growth and stress acclimation. However, the physiological significance of CRSH-dependent (p)ppGpp synthesis remains unclear, as no crsh-null mutant has been available. Here to investigate the function of CRSH, a crsh-knockout mutant of Arabidopsis was constructed using a site-specific gene-editing technique, and its phenotype was characterized. A transient increase of ppGpp was observed for 30 min in the wild type (WT) after light-to-dark transition, but this increase was not observed in the crsh mutant. Similar analyzes were performed with the rsh2rsh3 double and rsh1rsh2rsh3 triple mutants of Arabidopsis and showed that the transient increments of ppGpp in the mutants were higher than those in the WT. The increase of (p)ppGpp in the WT and rsh2rsh3 accompanied decrements in the mRNA levels of psbD transcribed by the plastid-encoded plastid RNA polymerase. These results indicated that the transient increase of intracellular ppGpp at night is due to CRSH-dependent ppGpp synthesis and the (p)ppGpp level is maintained by the hydrolytic activities of RSH1, RSH2, and RSH3 to accustom plastidial gene expression to darkness. expression Plants were grown on 0.8% agar-solidified 1/2 MS medium under continuous light (40 µmol photons m −2 s −1 ). Fourteen-day-old plants were transferred to the dark and ~0.1 g shoots were harvested at each of the time points indicated (Fig. 3). Extraction and quantification of ppGpp were as described previously . Western blot analysisProtein content was measured using the Bradford assay Kit (Bio Lab). Total proteins (6 µg each) were applied to an SDS-PAGE gel and electroblotted onto a polyvinylidene difluoride membrane (GE-Healthcare). The membrane was incubated with the CRSH-specific antibody . Immunoreactive proteins were detected using the Alkaline Phosphatase Substrate Kit II (Vector Laboratories).

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Significance of accumulation of the alarmone (p)ppGpp in chloroplasts for controlling photosynthesis and metabolite balance during nitrogen starvation in Arabidopsis

Cited by 33 publications

References 41 publications

Within and beyond the stringent response-RSH and (p)ppGpp in plants

Within and beyond the stringent response-RSH and (p)ppGpp in plants

ppGpp influences protein protection, growth and photosynthesis in Phaeodactylum tricornutum

Plastidial (p)ppGpp synthesis by the Ca²⁺-dependent RelA-SpoT homolog regulates the adaptation of chloroplast gene expression to darkness in Arabidopsis

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Significance of accumulation of the alarmone (p)ppGpp in chloroplasts for controlling photosynthesis and metabolite balance during nitrogen starvation in Arabidopsis

Cited by 33 publications

References 41 publications

Within and beyond the stringent response-RSH and (p)ppGpp in plants

Within and beyond the stringent response-RSH and (p)ppGpp in plants

ppGpp influences protein protection, growth and photosynthesis in Phaeodactylum tricornutum

Plastidial (p)ppGpp synthesis by the Ca2+-dependent RelA-SpoT homolog regulates the adaptation of chloroplast gene expression to darkness in Arabidopsis

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Plastidial (p)ppGpp synthesis by the Ca²⁺-dependent RelA-SpoT homolog regulates the adaptation of chloroplast gene expression to darkness in Arabidopsis