Cytosolic ppGpp accumulation induces retarded plant growth and development

Ihara, Yuta; Masuda, Shinji

doi:10.1080/15592324.2015.1132966

Cited by 12 publications

(9 citation statements)

References 17 publications

(20 reference statements)

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“…Arabidopsis transgenic plants that overexpress inducible B. subtilis yjbM— coding a (p)ppGpp synthetase that due to the lack of transit peptide is supposed to localize in cytoplasm—produce 10–20-fold higher levels of (p)ppGpp and display reduced fresh weight (about 20%) in comparison to WT plants. Hence, the authors proposed that depending on plastidial or cytosolic localization, (p)ppGpp either promotes or restrains plant growth, respectively, by regulating gene expression and metabolic processes to optimize growth in changing environmental conditions (Ihara and Masuda 2016 ). However, no localization studies of the YjbM protein in the Arabidopsis transgenic line were performed, leaving open the possibility of its plastidial functioning.…”

Section: Alarmones In Cytoplasmmentioning

confidence: 99%

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: Alarmones In Cytoplasmmentioning

confidence: 99%

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

Boniecka

Prusińska

Dąbrowska

et al. 2017

Planta

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“…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. The artificial accumulation of (p)ppGpp in the cytosol induces a dwarf phenotype in Arabidopsis (Ihara and Masuda 2016), which indicates that the (p)ppGpp-dependent stringent response may function in the cytosol; however, this hypothesis requires confirmation.…”

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. 2020

Plant and Cell Physiology

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In bacteria, the hyper-phosphorylated nucleotide, guanosine 3′,5′-bis(pyrophosphate) (ppGpp), functions as a secondary messenger under stringent conditions. ppGpp levels are controlled by two distinct enzymes, namely RelA and SpoT, in Escherichia coli. RelA–SpoT homologs (RSHs) are also conserved in plants where they function in the plastids. The model plant Arabidopsis thaliana contains four RSHs: RSH1, RSH2, RSH3 and Ca2+-dependent RSH (CRSH). Genetic characterizations of RSH1, RSH2 and RSH3 were undertaken, which showed that the ppGpp-dependent plastidial stringent response significantly influences plant growth and stress acclimation. However, the physiological significance of CRSH-dependent 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 in ppGpp was observed for 30 min in the wild type (WT) after the light-to-dark transition, but this increase was not observed in the crsh mutant. Similar analyses were performed with the rsh2-rsh3 double and rsh1-rsh2-rsh3 triple mutants and showed that the transient increments of ppGpp in the mutants were higher than those in the WT. The increase in ppGpp in the WT and rsh2 rsh3 accompanied decrements in the mRNA levels of some plastidial genes transcribed by the plastid-encoded plastid RNA polymerase. These results indicate that the transient increase in ppGpp at night is due to CRSH-dependent ppGpp synthesis and that the ppGpp level is maintained by the hydrolytic activities of RSH1, RSH2 and RSH3 to accustom plastidial gene expression to darkness.

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“…The UAS-yjbM (residues 1–636 with a C-terminal FLAG tag) fly was produced as follows. At first, B. subtilis yjbM was amplified with a primer pair, 5′-AGGGAATTGGGAATTCAAAATGGATGACAAACAGTGG-3′ and 5′-ATCTGTTAACGAATTCTTACTTATCATCATCATCCTTATAATC-3′, and synthesized yjbM gene 54 as a template. The amplified fragment was cloned into EcoRI-cut pUASTattB 55 by In-fusion cloning kit (Clontech), which was integrated into the specific site (VK31) of chromosome III with the Φ C31 system 55 .…”

Section: Methodsmentioning

confidence: 99%

“…For the experiment, pppGpp standard 12 was prepared as follows. At first, B. subtilis yjbM was amplified with a primer pair, 5′-AAGGAGATATACATATGGATGACAAACAGTGGG-3′ and 5′-GGTGGTGGTGCTCGAGTTGCTGCTCAGATCCTTTC-3′, and synthesized yjbM gene 54 as a template. The amplified fragment was cloned into Nde I- Xho I-cut pET29a (Merck) by In-fusion cloning kit (Clontech).…”

Section: Methodsmentioning

confidence: 99%

ppGpp functions as an alarmone in metazoa

et al. 2020

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Guanosine 3′,5′-bis(pyrophosphate) (ppGpp) functions as a second messenger in bacteria to adjust their physiology in response to environmental changes. In recent years, the ppGpp-specific hydrolase, metazoan SpoT homolog-1 (Mesh1), was shown to have important roles for growth under nutrient deficiency in Drosophila melanogaster. Curiously, however, ppGpp has never been detected in animal cells, and therefore the physiological relevance of this molecule, if any, in metazoans has not been established. Here, we report the detection of ppGpp in Drosophila and human cells and demonstrate that ppGpp accumulation induces metabolic changes, cell death, and eventually lethality in Drosophila. Our results provide the evidence of the existence and function of the ppGpp-dependent stringent response in animals.

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Cytosolic ppGpp accumulation induces retarded plant growth and development

Cited by 12 publications

References 17 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

Plastidial (p)ppGpp Synthesis by the Ca2+-Dependent RelA–SpoT Homolog Regulates the Adaptation of Chloroplast Gene Expression to Darkness in Arabidopsis

ppGpp functions as an alarmone in metazoa

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