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TOR coordinates nucleotide availability with ribosome biogenesis in plants

View ORCID ProfileMichael Busche, View ORCID ProfileM. Regina Scarpin, View ORCID ProfileRobert Hnasko, View ORCID ProfileJacob O. Brunkard
doi: https://doi.org/10.1101/2020.01.30.927418
Michael Busche
1Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720
2Plant Gene Expression Center, USDA Agricultural Research Service, Albany, CA 94710
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  • ORCID record for Michael Busche
M. Regina Scarpin
1Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720
2Plant Gene Expression Center, USDA Agricultural Research Service, Albany, CA 94710
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Robert Hnasko
3Produce Safety and Microbiology Research Unit, Western Regional Research Center, Pacific West Area, USDA Agricultural Research Service
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Jacob O. Brunkard
1Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720
2Plant Gene Expression Center, USDA Agricultural Research Service, Albany, CA 94710
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  • For correspondence: brunkard@berkeley.edu
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ABSTRACT

TARGET OF RAPAMYCIN (TOR) is a conserved eukaryotic Ser/Thr protein kinase that coordinates growth and metabolism with nutrient availability. We conducted a medium-throughput functional genetic screen to discover essential genes that promote TOR activity in plants, and identified a critical regulatory enzyme, cytosolic phosphoribosyl pyrophosphate (PRPP) synthetase (PRS4). PRS4 synthesizes cytosolic PRPP, a key upstream metabolite in nucleotide synthesis and salvage pathways. We found that prs4 knockouts are embryo-lethal in A. thaliana, and that silencing PRS4 expression in N. benthamiana causes pleiotropic developmental phenotypes, including dwarfism, aberrant leaf shape, and delayed flowering. Transcriptomic analysis revealed that ribosome biogenesis is among the most strongly repressed processes in prs4 knockdowns. Building on these results, we discovered that TOR activity is inhibited by chemical or genetic disruption of nucleotide biosynthesis, but that this effect can be reversed by supplying plants with physiological levels of nucleotides. Finally, we show that TOR transcriptionally promotes nucleotide biosynthesis to support the demands of ribosomal RNA synthesis. We propose that TOR coordinates ribosome biogenesis with nucleotide availability in plants to maintain metabolic homeostasis and support growth.

Footnotes

  • The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is Jacob O. Brunkard (brunkard{at}berkeley.edu).

  • Author list updated.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted February 04, 2020.
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TOR coordinates nucleotide availability with ribosome biogenesis in plants
Michael Busche, M. Regina Scarpin, Robert Hnasko, Jacob O. Brunkard
bioRxiv 2020.01.30.927418; doi: https://doi.org/10.1101/2020.01.30.927418
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TOR coordinates nucleotide availability with ribosome biogenesis in plants
Michael Busche, M. Regina Scarpin, Robert Hnasko, Jacob O. Brunkard
bioRxiv 2020.01.30.927418; doi: https://doi.org/10.1101/2020.01.30.927418

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