Impact of the plastidial stringent response in plant growth and stress responses

Maekawa, M.; Honoki, Rina; Ihara, Yuta; Satō, Ryōichi; Oikawa, Akira; Kanno, Yuka; Ohta, Hiroyuki; Seo, Mitsunori; Saito, Kazuki; Masuda, Shinji

doi:10.1038/nplants.2015.167

Cited by 54 publications

(162 citation statements)

References 47 publications

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“…Overexpression lines have strong basal chlorophyll fluorescence, F0 ( Figure 1A; Supplemental Figure 3), and a reduction in the maximal efficiency (or quantum yield, QY) of photosystem II (PSII): the average quantum yield was 0.86 6 0.001 SE in wild-type plants 12 d after stratification (DAS) versus 0.690 6 0.002 SE in OX: RSH2-GFP.1, 0.69 6 0.006 SE in OX:RSH3-GFP.1, and 0.73 6 0.006 SE in OX:RSH3-GFP.2 (n = 8). During preparation of this manuscript, similar phenotypes were reported for plant lines overexpressing RSH3 (Maekawa et al, 2015). Now focusing on plants overexpressing RSH3-GFP, we confirmed that chlorophyll levels are lower than in wild-type plants and found that this is accompanied by a reduction in the chlorophyll a/b ratio ( Figure 1B).…”

Section: Results Ppgpp Regulates Global Chloroplast Functionsupporting

confidence: 67%

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: Results Ppgpp Regulates Global Chloroplast Functionsupporting

confidence: 67%

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

et al. 2016

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“…The lower levels of photosynthetic pigments in ppGpp + cells could be due to increased pigment degradation, decreased pigment production, or a combination of the two. Based on these results, it is likely that ppGpp + cells are less photosynthetically active than control cells (18,19).…”

Section: High (P)ppgpp Levels Stop Growth and Dramatically Alter Synementioning

confidence: 99%

“…In Arabidopsis thaliana, all of these proteins localize to the chloroplast (19,56), and ppGpp levels rise in plants in response to darkness and other stresses, including wounding (57). Two recent studies have also shown that ppGpp levels affect photosynthetic capacity and chloroplast development in Arabidopsis (19,58). Thus, it is likely that aspects of the stringent response pathway are conserved between cyanobacteria and chloroplasts.…”

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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“…9 The ppGpp effects on plant growth are the opposite of those observed in the cytosolic ppGpp overaccumulation mutant as reported here, suggesting that cytosolic and plastidial ppGpp levels could regulate plant growth in a different way. Perhaps, in the wild type plant, ppGpp levels are coordinately regulated in each location for optimizing different metabolic processes and gene expressions to adapt the growth rate in response to varying environmental conditions.…”

mentioning

confidence: 57%

“…We recently showed that Arabidopsis RSHs, localized in chloroplasts, are important for plant growth and stress responses; ppGpp overaccumulation in chloroplasts results in robust growth under nutrient-deficient conditions. 9 This indicates that the stringent response is at least operating in the organelle, which has important roles in the systematic growth of host organisms.…”

mentioning

confidence: 99%

Cytosolic ppGpp accumulation induces retarded plant growth and development

Ihara

Masuda

2016

Plant Signaling & Behavior

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In bacteria a second messenger, guanosine 5 0 -diphosphate 3 0 -diphosphate (ppGpp), synthesized upon nutrient starvation, controls many gene expressions and enzyme activities, which is necessary for growth under changeable environments. Recent studies have shown that ppGpp synthase and hydrolase are also conserved in eukaryotes, although their functions are not well understood. We recently showed that ppGpp-overaccumulation in Arabidopsis chloroplasts results in robust growth under nutrient-limited conditions, demonstrating that the bacterial-like stringent response at least functions in plastids. To test if ppGpp also functions in the cytosol, we constructed the transgenic Arabidopsis expressing Bacillus subtilis ppGpp synthase gene yjbM. Upon induction of the gene, the mutant synthesizes »10-20-fold higher levels of ppGpp, and its fresh weight was reduced to~80% that of the wild type. These results indicate that cytosolic ppGpp negatively regulates plant growth and development.

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Impact of the plastidial stringent response in plant growth and stress responses

Cited by 54 publications

References 47 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

Cytosolic ppGpp accumulation induces retarded plant growth and development

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