Novel insights into the role of long non-coding RNA in the human malaria parasite, Plasmodium falciparum

Gayani Batugedara, Xueqing M. Lu, Borislav Hristov, Steven Abel, Zeinab Chahine, Thomas Hollin, Desiree Williams, Tina Wang, Anthony Cort, Todd Lenz, Trevor A. Thompson, Jacques Prudhomme, Abhai K. Tripathi, Guoyue Xu, Juliana Cudini, Sunil Dogga, Mara Lawniczak, William Stafford Noble, Photini Sinnis and Karine G. Le Roch ()
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Gayani Batugedara: University of California Riverside
Xueqing M. Lu: University of California Riverside
Borislav Hristov: University of Washington
Steven Abel: University of California Riverside
Zeinab Chahine: University of California Riverside
Thomas Hollin: University of California Riverside
Desiree Williams: University of California Riverside
Tina Wang: University of California Riverside
Anthony Cort: University of California Riverside
Todd Lenz: University of California Riverside
Trevor A. Thompson: University of California Riverside
Jacques Prudhomme: University of California Riverside
Abhai K. Tripathi: Johns Hopkins Bloomberg School of Public Health
Guoyue Xu: Johns Hopkins Bloomberg School of Public Health
Juliana Cudini: Wellcome Sanger Institute
Sunil Dogga: Wellcome Sanger Institute
Mara Lawniczak: Wellcome Sanger Institute
William Stafford Noble: University of Washington
Photini Sinnis: Johns Hopkins Bloomberg School of Public Health
Karine G. Le Roch: University of California Riverside

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: Abstract The complex life cycle of Plasmodium falciparum requires coordinated gene expression regulation to allow host cell invasion, transmission, and immune evasion. Increasing evidence now suggests a major role for epigenetic mechanisms in gene expression in the parasite. In eukaryotes, many lncRNAs have been identified to be pivotal regulators of genome structure and gene expression. To investigate the regulatory roles of lncRNAs in P. falciparum we explore the intergenic lncRNA distribution in nuclear and cytoplasmic subcellular locations. Using nascent RNA expression profiles, we identify a total of 1768 lncRNAs, of which 718 (~41%) are novels in P. falciparum. The subcellular localization and stage-specific expression of several putative lncRNAs are validated using RNA-FISH. Additionally, the genome-wide occupancy of several candidate nuclear lncRNAs is explored using ChIRP. The results reveal that lncRNA occupancy sites are focal and sequence-specific with a particular enrichment for several parasite-specific gene families, including those involved in pathogenesis and sexual differentiation. Genomic and phenotypic analysis of one specific lncRNA demonstrate its importance in sexual differentiation and reproduction. Our findings bring a new level of insight into the role of lncRNAs in pathogenicity, gene regulation and sexual differentiation, opening new avenues for targeted therapeutic strategies against the deadly malaria parasite.

Date: 2023
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DOI: 10.1038/s41467-023-40883-w

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