Updated project metadata. Chloroplasts are the powerhouse of the plant cell, and their activity must be matched to plant growth to avoid photo-oxidative damage. We have identified a post-translational mechanism linking the conserved Target of Rapamycin (TOR) kinase that promotes growth and the guanosine tetraphosphate (ppGpp) signaling pathway that regulates chloroplast activity, and photosynthesis in particular. We find that RelA SpoT Homologue 3 (RSH3), a nuclear-encoded enzyme responsible for ppGpp biosynthesis, interacts directly with the TOR complex via a plant-specific N-terminal region which is phosphorylated in a TOR-dependent manner. Downregulating TOR activity increases ppGpp synthesis by RSH3, and reduces photosynthetic capacity. The TOR-RSH3 signaling axis therefore regulates chloroplast activity to match plant growth, and sets a new precedent for the regulation of organellar function by TOR.