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

Abstract

The regulatory nucleotide guanosine 5′-diphosphate 3′-diphosphate (ppGpp), which was originally identified in Escherichia coli, controls the expression of a large gene set and many enzyme activities. The ppGpp-dependent control of cell activities is referred to as the stringent response. Recently, genes responsible for the synthesis and degradation of ppGpp have been identified not only in bacteria, but also in eukaryotes, including plants and animals, indicating that the stringent response is, unexpectedly, widely conserved. However, the exact function of the eukaryotic stringent response remains elusive. Here, we isolated an Arabidopsis mutant that overproduces ppGpp in chloroplasts. This mutant shows metabolite reduction, dwarf chloroplasts and significantly suppressed plastidial transcription and translation. Under nutrient-deficient conditions, the mutant shows more robust growth than the wild type. These results indicate that the ppGpp-dependent control of the organelle function is crucial for the systematic growth of host organisms.

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Figure 1: Phenotypes of RSH2- and RSH3-overexpression lines.
Figure 2: Chloroplast structure in the mutants.
Figure 3: Lipid profiles, metabolic changes and plastidial gene expression in rsh mutants.
Figure 4: ppGpp accumulation results in tolerance to nutrient starvation.

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Acknowledgements

We thank R. Sasaki (RIKEN) , K. Yamamichi (Tokyo Institute of Technology) and K. Hori (Tokyo Institute of Technology) for excellent technical assistance, L. Kwok (Tokyo Institute of Technology) for critical reading of the manuscript, and T. Hisabori (Tokyo Institute of Technology), Y. Nagano (Saga University) and M. Ikeuchi (The University of Tokyo) for antibodies. We also thank the Arabidopsis Biological Resource Center (The Ohio State University) for providing mutant seeds. This work was supported by a Grants-in-Aid for Scientific Research on Innovative Areas from MEXT of Japan (No. 25120709) to S.M.

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M.M. and R.H. performed phenotypic analysis of mutants that includes gene expression analysis, immunoblot analysis, photosynthetic activity measurements and lipid analysis. Y.I. performed ppGpp quantification. R.S. analysed localization of GFP fusion proteins. R.H. and A.O. performed metabolome analysis, Y.K. and M.S. performed hormone quantification. All authors analysed data and discussed the results. S.M. designed the research. M.M. and S.M. wrote the article.

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Correspondence to Shinji Masuda.

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Maekawa, M., Honoki, R., Ihara, Y. et al. Impact of the plastidial stringent response in plant growth and stress responses. Nature Plants 1, 15167 (2015). https://doi.org/10.1038/nplants.2015.167

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