Abstract
BackgroundFollowing fertilization, the early proteomes of metazoans are defined by the translation of stored but repressed transcripts; further embryonic development relies on de novo transcription of the zygotic genome. During sexual development of Plasmodium berghei, a rodent model for human malaria species including P. falciparum, the stability of repressed mRNAs requires the translational repressors DOZI and CITH. When these repressors are absent, Plasmodium zygote development and transmission to the mosquito vector is halted, as hundreds of transcripts become destabilized. However, which mRNAs are direct targets of these RNA binding proteins, and thus subject to translational repression, is unknown.ResultsWe identify the maternal mRNA contribution to post-fertilization development of P. berghei using RNA immunoprecipitation and microarray analysis. We find that 731 mRNAs, approximately 50% of the transcriptome, are associated with DOZI and CITH, allowing zygote development to proceed in the absence of RNA polymerase II transcription. Using GFP-tagging, we validate the repression phenotype of selected genes and identify mRNAs relying on the 5′ untranslated region for translational control. Gene deletion reveals a novel protein located in the ookinete crystalloid with an essential function for sporozoite development.ConclusionsOur study details for the first time the P. berghei maternal repressome. This mRNA population provides the developing ookinete with coding potential for key molecules required for life-cycle progression, and that are likely to be critical for the transmission of the malaria parasite from the rodent and the human host to the mosquito vector.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-014-0493-0) contains supplementary material, which is available to authorized users.
Highlights
Following fertilization, the early proteomes of metazoans are defined by the translation of stored but repressed transcripts; further embryonic development relies on de novo transcription of the zygotic genome
Presenting the first RIP-Chip approach for Plasmodium, we demonstrate that zygote morphogenesis is largely transcription-independent and driven by maternal factors contained in Development Of Zygote Inhibited (DOZI)/CAR-I and Trailer Hitch Homolog (CITH) Messenger ribonucleoprotein (mRNP); our data reveal specific groups of maternal transcripts whose encoded proteins are responsible for the morphological and functional changes observed during zygote-to-ookinete transition
Using in situ tagging of five RIP-identified genes with GFP, we show that translational repression is dependent on 5′ untranslated regions (UTRs) rather than 3′ Untranslated regions (UTR), and identify a novel crystalloid protein that plays an essential role for sporogony to occur
Summary
The early proteomes of metazoans are defined by the translation of stored but repressed transcripts; further embryonic development relies on de novo transcription of the zygotic genome. During sexual development of Plasmodium berghei, a rodent model for human malaria species including P. falciparum, the stability of repressed mRNAs requires the translational repressors DOZI and CITH When these repressors are absent, Plasmodium zygote development and transmission to the mosquito vector is halted, as hundreds of transcripts become destabilized. Fertilization of the immotile female by a flagellated male results in the formation of a round, diploid zygote that within 18 to 24 h transforms into a morphologically distinct cell type: the elongated and motile and unicellular ookinete This specialized cell escapes the blood meal by penetrating the peritrophic membrane surrounding the blood meal, traverses the midgut epithelium and establishes the replicating oocyst that can give rise to thousands of sporozoites
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