The eIF3e subunit form an octameric ribonucleoprotein complex to initiate translation, and its PCI domain engage in the assembly of the proteolytic 26S proteosome supercomplex. These two complexes are central in translation initiation and protein quality surveillance and turnover. However, how eIF3e is structurally regulated remain unknown. Here, using RIPseq approach we revealed that eIF3e co-immunoprecipitate with mRNAs involved in RNA biosynthesis (U3 snRNA12a and ncRNA processing) and cell morphology, and its PCI domain is crucial for regulation of pollen tube pulse growth and eIF3e dissociation post initiation. We show that motifs within eIF3e associated target RNAs can repress or activate translation. Since the PCI domain associate with the proteosome machinery, we show that pharmacological inhibition of the proteosome complex accumulate eIF3e, eIF3eΔPCI and the proteosome lid subunits RPN7/RPN12a to the nucleus and generate nuclear condensates. Importantly, constitutive dephosphorylation of eIF3e revealed antagonistic phosphosites at the PCI domain that balance pollen tube growth and cellular membrane morphology. These findings inform structural features that control eIF3e activities and that antagonistic de-phosphorylation of eIF3e maintain equilibrium of pollen tube growth rate dynamics and membrane structural morphology.