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How these important pathogens transition between insect and mammalian stages is only poorly understood. Here, we investigated stage differentiation in\n                    <jats:italic>Leishmania donovani<\/jats:italic>\n                    , a trypanosomatid parasite with constitutive gene transcription, offering a model to study post-transcriptional regulation. Using a five-layer integrative systems analysis (genome to metabolome), we compared hamster-derived amastigotes and culture-derived promastigotes. Genomic adaptation was excluded as a major driver of differentiation, while differential mRNA turnover emerged as a key mechanism of stage-specific gene expression. Transcriptomic and proteomic comparisons revealed a broad dynamic range of protein abundance changes that correlated poorly with mRNA levels. This discrepancy was linked to (i) altered snoRNA expression and rRNA modifications, indicating stage-specific tuning of translation, and (ii) differential protein degradation, supported by proteomics following proteasome inhibition with lactacystin. Lactacystin impaired amastigote-to-promastigote differentiation, highlighting the importance of proteasomal activity. Overall, our analysis links\n                    <jats:italic>Leishmania<\/jats:italic>\n                    development to coordinated post-transcriptional regulatory networks. Our findings provide a powerful new resource for research programs that aim to dissect the emergent properties of regulatory networks and feedback loops underlying\n                    <jats:italic>Leishmania<\/jats:italic>\n                    stage differentiation, serving as a blueprint for other vector-borne pathogens that rely on disease-associated developmental transitions.\n                  <\/jats:p>","DOI":"10.7554\/elife.111115","type":"journal-article","created":{"date-parts":[[2026,4,15]],"date-time":"2026-04-15T14:30:32Z","timestamp":1776263432000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.111115","source":"Crossref","is-referenced-by-count":0,"title":["Five-layer systems analysis of Leishmania stage differentiation reveals an essential role for protein degradation in parasite 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