The ErbB-3 BINDING PROTEIN 1 (EBP1) drives growth, however, the mechanism of how it acts in plants is little understood. We show that EBP1 expression and protein abundance are predominantly confined to meristematic cells, induced by sucrose and partly dependent on TARGET OF RAPAMYCIN (TOR) kinase activity. Consistent with being downstream to TOR, silencing of EBP1 restrains, while overexpression promotes root growth mostly under sucrose-limiting conditions. RETINOBLASTOMA RELATED (RBR) is a sugar-dependent transcriptional repressor of cell proliferation. Inducible RBR overexpression depletes meristematic activity and causes precocious differentiation, which is attenuated by EBP1. To understand the molecular mechanism, we searched for EBP1- and RBR-interacting proteins by affinity purification and mass spectrometry. In line with the dsRNA-binding activity of EBP1 in human cells, the overwhelming majority of EBP1 interactors are part of ribonucleoprotein complexes regulating many aspects of protein synthesis, including ribosome biogenesis and mRNA translation. We confirmed that EBP1 associates with ribosomes and that EBP1 silencing hinders the rRNA processing. Unexpectedly, we revealed that RBR also interacts with a set of EBP1-associated nucleolar proteins as well as factors that function in protein translation. This suggests that EBP1 and RBR act antagonistically on common processes that determine the capacity for translation to tune meristematic activity in relation to available resources.