Diversity in Guanosine 3′,5′-Bisdiphosphate (ppGpp) Sensitivity among Guanylate Kinases of Bacteria and Plants

Nomura, Yuhta; Izumi, Atsushi; Fukunaga, Yoshinori; Kusumi, Kensuke; Iba, Koh; Watanabe, Shizuo; Nakahira, Yoichi; Weber, Andreas P.M.; Nozawa, Akira; Tozawa, Yuzuru

doi:10.1074/jbc.m113.534768

Cited by 36 publications

(43 citation statements)

References 35 publications

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“…This shows that the main characteristics of the stringent response are conserved between plants and bacteria. We also propose on the basis of the data that we present here, the in vitro sensitivity of plant GKs to ppGpp (Nomura et al, 2014), and the GTP initiation of plant rRNA genes (Suzuki et al, 2003;Swiatecka-Hagenbruch et al, 2007) that ppGpp is most likely to inhibit transcription by a similar mechanism to that found in B. subtilis.…”

Section: Discussionmentioning

confidence: 93%

“…Chloroplasts also contain an alternative Nucleus-Encoded Polymerase (NEP), which plays a minor role in green tissues and is not inhibited by ppGpp. A recent study also provides support for a B. subtilis-like mechanism by showing that recombinant chloroplastic GK enzymes from rice (Oryza sativa) and Arabidopsis are as sensitive to inhibition by ppGpp in vitro as the B. subtilis GK with IC50s of around 30 µM (Nomura et al, 2014).…”

Section: Ppgpp Regulates Chloroplast Gene Expression By Reducing Steamentioning

confidence: 99%

“…Studies using purified chloroplast enzymes and chloroplast extracts suggest that ppGpp may function in planta by inhibiting translation and/or transcription in a manner analogous to the bacterial stringent response (Takahashi et al, 2004;Sato et al, 2009;Masuda, 2012;Nomura et al, 2012;Nomura et al, 2014). However, there remains substantial uncertainty about both the principal targets and effects of ppGpp in the plant under physiological conditions.…”

Section: Introductionmentioning

confidence: 99%

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An Ancient Bacterial Signaling Pathway Regulates Chloroplast Function to Influence Growth and Development in Arabidopsis

et al. 2016

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The chloroplast originated from the endosymbiosis of an ancient photosynthetic bacterium by a eukaryotic cell. Remarkably, the chloroplast has retained elements of a bacterial stress response pathway that is mediated by the signaling nucleotides guanosine penta-and tetraphosphate (ppGpp). However, an understanding of the mechanism and outcomes of ppGpp signaling in the photosynthetic eukaryotes has remained elusive. Using the model plant Arabidopsis thaliana, we show that ppGpp is a potent regulator of chloroplast gene expression in vivo that directly reduces the quantity of chloroplast transcripts and chloroplast-encoded proteins. We then go on to demonstrate that the antagonistic functions of different plant RelA SpoT homologs together modulate ppGpp levels to regulate chloroplast function and show that they are required for optimal plant growth, chloroplast volume, and chloroplast breakdown during dark-induced and developmental senescence. Therefore, our results show that ppGpp signaling is not only linked to stress responses in plants but is also an important mediator of cooperation between the chloroplast and the nucleocytoplasmic compartment during plant growth and development.

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Section: Discussionmentioning

confidence: 93%

Section: Ppgpp Regulates Chloroplast Gene Expression By Reducing Steamentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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An Ancient Bacterial Signaling Pathway Regulates Chloroplast Function to Influence Growth and Development in Arabidopsis

et al. 2016

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“…This analysis does not predict a mechanism for the stringent response in cyanobacteria, but several observations suggest that neither of these strategies fully accounts for the global regulation enacted by (p)ppGpp in Synechococcus. In vitro assays with Synechococcus GMK have shown that it is insensitive to (p)ppGpp (41), and its genome lacks CodY and DksA homologs as well as the (p)ppGpp-interacting motif on RNA polymerase (42). Although it is likely that alteration of GTP pools as a result of (p)ppGpp synthesis could affect cell physiology and metabolic processes, we did not observe dramatic decreases in rRNA precursor levels when (p)ppGpp levels were high (SI Appendix, Fig.…”

Section: Conservation and Adaptation Of Stringent Response Mechanisms Inmentioning

confidence: 99%

The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus

Hood

Higgins

Flamholz

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

106

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The cyanobacterium Synechococcus elongatus relies upon photosynthesis to drive metabolism and growth. During darkness, Synechococcus stops growing, derives energy from its glycogen stores, and greatly decreases rates of macromolecular synthesis via unknown mechanisms. Here, we show that the stringent response, a stress response pathway whose genes are conserved across bacteria and plant plastids, contributes to this dark adaptation. Levels of the stringent response alarmone guanosine 3′-diphosphate 5′-diphosphate (ppGpp) rise after a shift from light to dark, indicating that darkness triggers the same response in cyanobacteria as starvation in heterotrophic bacteria. High levels of ppGpp are sufficient to stop growth and dramatically alter many aspects of cellular physiology, including levels of photosynthetic pigments and polyphosphate, DNA content, and the rate of translation. Cells unable to synthesize ppGpp display pronounced growth defects after exposure to darkness. The stringent response regulates expression of a number of genes in Synechococcus, including ribosomal hibernation promoting factor (hpf), which causes ribosomes to dimerize in the dark and may contribute to decreased translation. Although the metabolism of Synechococcus differentiates it from other model bacterial systems, the logic of the stringent response remains remarkably conserved, while at the same time having adapted to the unique stresses of the photosynthetic lifestyle.

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“…17) Recently, ppGpp was shown to inhibit guanylate kinase, an important enzyme in guanine nucleotide biosynthesis, in chloroplasts of plants. 18) On the other hand, nucleoside diphosphates linked to some moiety X (Nudix) hydrolases, AtNUDXs, has been shown to have ppGpp pyrophosphohydrolase activity in A. thaliana. The metabolic pathway of ppGpp without RelA/SpoT protein is shown to exist in plants.…”

Section: )mentioning

confidence: 99%

Overexpression of RelA/SpoT homologs, PpRSH2a and PpRSH2b, induces the growth suppression of the moss Physcomitrella patens

Sato

Takahashi

Ochi

et al. 2015

Bioscience, Biotechnology, and Biochemistry

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Two genes encoding RelA/SpoT homologs, PpRSH2a and PpRSH2b, which are involved in the synthesis of bacterial alarmone guanosine 5′-diphosphate 3′-diphosphate (ppGpp) for the stringent response, were isolated from the moss, Physcomitrella patens. A complementary analysis of PpRSH2a and PpRSH2b in Escherichia coli showed that these genes had ppGpp biosynthetic activity. The recombinant PpRSH2a and PpRSH2b were also shown to synthesize ppGpp in vitro. Both proteins were localized to the chloroplasts of P. patens. Expression of the PpRSH genes was induced upon treatment with abscisic acid or abiotic stresses, such as dehydration and UV irradiation. Overexpression of PpRSH2a and PpRSH2b caused suppression of the growth in response to 1% (w/v) of glucose. The present study suggests the existence of a mechanism to regulate the growth of P. patens, which is governed by plant RSH in chloroplasts

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Diversity in Guanosine 3′,5′-Bisdiphosphate (ppGpp) Sensitivity among Guanylate Kinases of Bacteria and Plants

Cited by 36 publications

References 35 publications

An Ancient Bacterial Signaling Pathway Regulates Chloroplast Function to Influence Growth and Development in Arabidopsis

An Ancient Bacterial Signaling Pathway Regulates Chloroplast Function to Influence Growth and Development in Arabidopsis

The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus

Overexpression of RelA/SpoT homologs, PpRSH2a and PpRSH2b, induces the growth suppression of the moss Physcomitrella patens

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