An axonemal intron splicing program sustains Plasmodium male development

Jiepeng Guan, Peijia Wu, Xiaoli Mo, Xiaolong Zhang, Wenqi Liang, Xiaoming Zhang, Lubin Jiang (), Jian Li (), Huiting Cui () and Jing Yuan ()
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Jiepeng Guan: Xiamen University
Peijia Wu: Xiamen University
Xiaoli Mo: Xiamen University
Xiaolong Zhang: Chinese Academy of Sciences
Wenqi Liang: Xiamen University
Xiaoming Zhang: Xiamen University
Lubin Jiang: Chinese Academy of Sciences
Jian Li: Xiamen University
Huiting Cui: Xiamen University
Jing Yuan: Xiamen University

Nature Communications, 2024, vol. 15, issue 1, 1-20

Abstract: Abstract Differentiation of male gametocytes into flagellated fertile male gametes relies on the assembly of axoneme, a major component of male development for mosquito transmission of the malaria parasite. RNA-binding protein (RBP)-mediated post-transcriptional regulation of mRNA plays important roles in eukaryotic sexual development, including the development of female Plasmodium. However, the role of RBP in defining the Plasmodium male transcriptome and its function in male gametogenesis remains incompletely understood. Here, we performed genome-wide screening for gender-specific RBPs and identified an undescribed male-specific RBP gene Rbpm1 in the Plasmodium. RBPm1 is localized in the nucleus of male gametocytes. RBPm1-deficient parasites fail to assemble the axoneme for male gametogenesis and thus mosquito transmission. RBPm1 interacts with the spliceosome E complex and regulates the splicing initiation of certain introns in a group of 26 axonemal genes. RBPm1 deficiency results in intron retention and protein loss of these axonemal genes. Intron deletion restores axonemal protein expression and partially rectifies axonemal defects in RBPm1-null gametocytes. Further splicing assays in both reporter and endogenous genes exhibit stringent recognition of the axonemal introns by RBPm1. The splicing activator RBPm1 and its target introns constitute an axonemal intron splicing program in the post-transcriptional regulation essential for Plasmodium male development.

Date: 2024
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DOI: 10.1038/s41467-024-49002-9

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