Glucose-driven TOR–FIE–PRC2 signalling controls plant development

Ruiqiang Ye (), Meiyue Wang, Hao Du, Shweta Chhajed, Jin Koh, Kun-hsiang Liu, Jinwoo Shin, Yue Wu, Lin Shi, Lin Xu, Sixue Chen, Yijing Zhang and Jen Sheen ()
Additional contact information
Ruiqiang Ye: Massachusetts General Hospital
Meiyue Wang: Chinese Academy of Sciences
Hao Du: Massachusetts General Hospital
Shweta Chhajed: University of Florida
Jin Koh: University of Florida
Kun-hsiang Liu: Massachusetts General Hospital
Jinwoo Shin: Massachusetts General Hospital
Yue Wu: Massachusetts General Hospital
Lin Shi: Massachusetts General Hospital
Lin Xu: Chinese Academy of Sciences
Sixue Chen: University of Florida
Yijing Zhang: Chinese Academy of Sciences
Jen Sheen: Massachusetts General Hospital

Nature, 2022, vol. 609, issue 7929, 986-993

Abstract: Abstract Nutrients and energy have emerged as central modulators of developmental programmes in plants and animals1–3. The evolutionarily conserved target of rapamycin (TOR) kinase is a master integrator of nutrient and energy signalling that controls growth. Despite its key regulatory roles in translation, proliferation, metabolism and autophagy2–5, little is known about how TOR shapes developmental transitions and differentiation. Here we show that glucose-activated TOR kinase controls genome-wide histone H3 trimethylation at K27 (H3K27me3) in Arabidopsis thaliana, which regulates cell fate and development6–10. We identify FERTILIZATION-INDEPENDENT ENDOSPERM (FIE), an indispensable component of Polycomb repressive complex 2 (PRC2), which catalyses H3K27me3 (refs. 6–8,10–12), as a TOR target. Direct phosphorylation by TOR promotes the dynamic translocation of FIE from the cytoplasm to the nucleus. Mutation of the phosphorylation site on FIE abrogates the global H3K27me3 landscape, reprogrammes the transcriptome and disrupts organogenesis in plants. Moreover, glucose–TOR–FIE–PRC2 signalling modulates vernalization-induced floral transition. We propose that this signalling axis serves as a nutritional checkpoint leading to epigenetic silencing of key transcription factor genes that specify stem cell destiny in shoot and root meristems and control leaf, flower and silique patterning, branching and vegetative-to-reproduction transition. Our findings reveal a fundamental mechanism of nutrient signalling in direct epigenome reprogramming, with broad relevance for the developmental control of multicellular organisms.

Date: 2022
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DOI: 10.1038/s41586-022-05171-5

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