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The RNA Structurome in the Asexual Blood Stages of Malaria Pathogen Plasmodium falciparum

ABSTRACT: Plasmodium falciparum is a deadly human pathogen responsible for the devastating disease called malaria. In this study, we measured the differential accumulation of RNA secondary structures in coding and noncoding transcripts from the asexual developmental cycle in P. falciparum in human red blood cells. Our comprehensive analysis that combined high-throughput nuclease mapping of RNA structures by duplex RNA-seq, SHAPE-directed RNA structure validation, immunoaffinity purification and characterization of antisense RNAs collectively measured differentially base-paired RNA regions throughout the parasite’s development. Our mapping data not only aligned to a diverse pool of RNAs with known structures but also enabled us to identify new structural RNA regions in the malaria genome. On average, approximately 71% of the genes with secondary structures are found to be protein coding mRNAs. The mapping pattern of these base-paired RNAs corresponded to all regions of protein-coding mRNAs, including the 5’ UTR, CDS and 3’ UTR as well as the start and stop codons. Histone family genes which are known to form secondary structures in their mRNAs and transcripts from genes which are important for transcriptional and post-transcriptional control, such as the unique plant-like transcription factor family, ApiAP2, DNA/RNA binding protein, Alba3 and proteins important for RBC invasion and malaria cytoadherence also showed strong accumulation of duplex RNA reads in various asexual stages in P. falciparum. Intriguingly, our study determined a positive relationship between mRNA structural contents and translation efficiency in P. falciparum asexual blood stages, suggesting an essential role of RNA structural changes in malaria gene expression programs.

ORGANISM(S): Plasmodium falciparum

PROVIDER: GSE163965 | GEO | 2021/04/05

REPOSITORIES: GEO

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Project description:In summary, we present a systematic in silico screen for the conserved non-coding RNA structures by comparing the P. falciparum genome with seven other malaria species and describe 668 candidate RNA secondary structures. By combining microarray and northern data, we provide evidence for expression of 28 novel ncRNA candidates at the transcript level in the blood stages of P. falciparum, a subset of which show intra-erythrocytic stage-specificity for expression. Few of the expressed novel candidates appear to have similarity to functionally known ncRNAs characterised to-date. The ncRNA candidates that show a narrow phylogenetic distribution, such as the internal var-associated ncRNAs, may be involved in species-specific function. At present, we can not assign specific function to these novel ncRNAs, however, our study highlights the abundance of these novel ncRNA structures in P. falciparum and suggests important roles for these ncRNAs in cellular processes. Although the control of gene expression by mechanisms such as epigenetics, post-transcriptional gene regulation and transcript stability has been recently shown in Plasmodium, all the key cellular players in such types of non-conventional gene regulation in Plasmodium are yet to be identified. Taking cues from the functionally characterized components of the higher eukaryotic non-coding RNA populations, it is tempting to speculate that ncRNAs may, at least in part, be instrumental in gene regulation in P. falciparum. However, in contrast to the higher eukaryotes, the absence of a conventional RNAi pathway and its associated components in malaria suggests that these malaria-specific novel ncRNAs, where functional, must exert their role using novel pathways or mechanisms, possibly unique to malaria. It remains to be determined what fraction of the ncRNAs described here are involved in modulating expression of one or more genes or gene families in malaria and also the precise cellular function for them not only in the blood stages but also in the other life-cycle stages of P. falciparum.

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The RNA Structurome in the Asexual Blood Stages of Malaria Pathogen Plasmodium falciparum

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