Leishmania parasites lack pathways for de novo purine biosynthesis. The depletion of purines induces differentiation into virulent metacyclic forms. In vitro, the parasites can survive prolonged periods of purine withdrawal changing their morphology to long and slender cells with an extended flagellum, and decreasing their translation rates. Reduced translation leads to the appearance of discrete granules that contain LeishIF4E-3, one of the six eIF4E paralogs encoded by the Leishmania genome. We hypothesize that each is responsible for a different function during the life cycle. LeishIF4E-3 is a weak cap-binding protein paralog, but its involvement in translation under normal conditions cannot be excluded. However, in response to nutritional stress, LeishIF4E-3 concentrates in specific cytoplasmic granules. LeishIF4E-3 granulation can be induced by the independent elimination of purines, amino acids and glucose. As these granules contain mature mRNAs, we propose that these bodies store inactive transcripts until recovery from stress occurs. In attempt to examine the content of the nutritional stress-induced granules, they were concentrated over sucrose gradients and further pulled-down by targeting in vivo tagged LeishIF4E-3. Proteomic analysis highlighted granule enrichment with multiple ribosomal proteins, suggesting that ribosome particles are abundant in these foci, as expected in case of translation inhibition. RNA-binding proteins, RNA helicases and metabolic enzymes were also enriched in the granules, whereas no degradation enzymes or P-body markers were detected. The starvation-induced LeishIF4E-3-containing granules, therefore, appear to store stalled ribosomes and ribosomal subunits, along with their associated mRNAs. Following nutritional stress, LeishIF4E-3 becomes phosphorylated at position S75, located in its less-conserved N-terminal extension. The ability of the S75A mutant to form granules was reduced, indicating that cellular signaling regulates LeishIF4E-3 function., Author summary Cells respond to cellular stress by decreasing protein translation, to prevent the formation of partially folded or misfolded new polypeptides whose accumulation can be detrimental to living cells. Under such conditions, the cells benefit from storing inactive mRNAs and stalled ribosomal particles, to maintain their availability once conditions improve; dedicated granules offer a solution for such storage. Leishmania parasites are exposed to a variety of stress conditions as a natural part of their life cycle, including the nutritional stress that the parasites experience within the gut of the sandfly. Thus, Leishmania and related trypanosomatids serve as a good model system to investigate RNA fate during different stress conditions. Various granules appear in Leishmania and related organisms in response to different stress conditions. Here, we investigated how nutritional stress, in particular elimination of purines, induced the formation of granules that harbor a specific cap-binding protein, LeishIF4E-3. The starvation-induced LeishIF4E-3 containing granules consist of a variety of ribosomal proteins, along with RNA-binding proteins and mature mRNAs. We thus propose that Leishmania modulates the assembly of LeishIF4E-3-containing granules for transient storage of stalled ribosomal particles and inactive mRNAs. Following renewal of nutrient availability, as occurs during the parasite’s life cycle, the granules disappear. Although their fate is yet unclear, they could be recycled in the cell. Unlike other granules described in trypanosomes, the LeishIF4E-3-containing granules did not contain RNA degradation enzymes, suggesting that their function is mainly for storage until conditions improve.