Glucose–TOR signalling reprograms the transcriptome and activates meristems

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Abstract

Meristems encompass stem/progenitor cells that sustain postembryonic growth of all plant organs. How meristems are activated and sustained by nutrient signalling remains enigmatic in photosynthetic plants. Combining chemical manipulations and chemical genetics at the photoautotrophic transition checkpoint, we reveal that shoot photosynthesis-derived glucose drives target-of-rapamycin (TOR) signalling relays through glycolysis and mitochondrial bioenergetics to control root meristem activation, which is decoupled from direct glucose sensing, growth-hormone signalling and stem-cell maintenance. Surprisingly, glucose–TOR signalling dictates transcriptional reprogramming of remarkable gene sets involved in central and secondary metabolism, cell cycle, transcription, signalling, transport and protein folding. Systems, cellular and genetic analyses uncover TOR phosphorylation of E2Fa transcription factor for an unconventional activation of S-phase genes, and glucose-signalling defects in e2fa root meristems. Our findings establish pivotal roles of glucose–TOR signalling in unprecedented transcriptional networks wiring central metabolism and biosynthesis for energy and biomass production, and integrating localized stem/progenitor-cell proliferation through inter-organ nutrient coordination to control developmental transition and growth.

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Figure 1: Photosynthesis controls the metabolic activation of root meristems.
Figure 2: Glucose–TOR signalling in root meristems.
Figure 3: Auxin and cytokinin signalling and root stem-cell maintenance are decoupled from TOR activation.
Figure 4: Glucose–TOR signalling orchestrates transcriptome reprogramming.
Figure 5: TOR kinase phosphorylates and activates E2Fa.
Figure 6: TOR kinase controls the activity of E2Fa in transcriptional activation.

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Primary accessions

Gene Expression Omnibus

Data deposits

All microarray data are available at the Gene Expression Omnibus under accession number GSE40245.

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Acknowledgements

We thank N. Dai and J. Avruch for S6K antibodies and advice, J. L. Celenza for stimulating discussion, M. D. Curtis and Y. J. Niu for the oestradiol-inducible binary vector, L. Li and J. Bush for seeds and plants, B. Müller for TCS::GFP, J. Friml for DR5::GFP, N. S. Gray and D. M. Sabatini for torin1, and J. F. Li, H. Lee and M. Ramon for critical reading of the manuscript. Y.X. is supported by the MGH Tosteson Postdoctoral Fellowship. C.X. is supported by Chinese Academy of Sciences (KSCX3-YW-N-007). The Research is supported by the NSF, NIH and WJC Special Project (PJ009106) RDA-Korea to J.S.

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Authors

Contributions

Y.X. and J.S. initiated the project and designed the experiments; Y.X. carried out most of the experiments; L.L. and Y.X. conducted quantitative ChIP-PCR analyses; Y.X., M.M. and J.S. analysed the microarray data. C.X. isolated the e2fa mutant. Q.H. generated PLT::GFP and WOX5::GFP transgenic lines. Y.X., M.M. and J.S. wrote the manuscript.

Corresponding authors

Correspondence to Yan Xiong or Jen Sheen.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contain Supplementary Figures 1-22, legends for Supplementary Tables 1-2, 5-7 (see separate files for tables), Supplementary Tables 3-4, 8-11, Supplementary Methods and Supplementary References. (PDF 2819 kb)

Supplementary Table 1

This file contains the Glucose-TOR target genes – see Supplementary Information file for full legend. (XLSX 259 kb)

Supplementary Table 2

This file contains the Novel glucose regulated genes – see Supplementary Information file for full legend. (XLSX 47 kb)

Supplementary Table 5

This file contains the Glucose-TOR target gene list (P value <0.01) – see Supplementary Information file for full legend. (XLSX 426 kb)

Supplementary Table 6

This file contains the Glucose-TOR target genes involved in cell cycle – see Supplementary Information file for full legend. (XLSX 76 kb)

Supplementary Table 7

This file contains the Putative E2Fa target genes – see Supplementary Information file for full legend. (XLSX 367 kb)

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Xiong, Y., McCormack, M., Li, L. et al. Glucose–TOR signalling reprograms the transcriptome and activates meristems. Nature 496, 181–186 (2013). https://doi.org/10.1038/nature12030

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