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An axonemal intron splicing program sustains Plasmodium male development

ABSTRACT: To gain further insights into the post-transcriptional regulation process in the male sexual stage of Plasmodium, we focused on RBPm1, the most specifically expressed RNA-binding protein in the male gametocyte of P. yoelii, for in-depth investigation. In the first part of this study, we identified RBPm1 as a splicing activator, facilitating the splicing of 30 introns among 26 genes in the male gametocytes. Next, we sought to elucidate how RBPm1 exerts its splicing-promoting function. To achieve this, we performed biotin-based proximity labeling experiments on RBPm1, identifying 113 proteins that interact with RBPm1. Among these proteins, all 13 subunits of the spliceosome E complex were present, while other components of the splicing cycle were not significantly enriched. This suggests that RBPm1 participates in the initiation step of RNA splicing by interacting with the E-complex to promote intron splicing.

ORGANISM(S): Plasmodium Yoelii Yoelii 17xnl

SUBMITTER: Jing Yuan

PROVIDER: PXD044094 | iProX | Wed Jul 26 00:00:00 BST 2023

REPOSITORIES: iProX

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An axonemal intron splicing program sustains Plasmodium male development.

Guan Jiepeng J Wu Peijia P Mo Xiaoli X Zhang Xiaolong X Liang Wenqi W Zhang Xiaoming X Jiang Lubin L Li Jian J Cui Huiting H Yuan Jing J

Nature communications 20240601 1

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 incom ...[more]

PMID: 38824128

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Project description:The transmission of the malaria parasite between mosquitoes and mammals requires translational repression to ensure that only the proper proteins are expressed at the right time, while still allowing the parasite to prepare the mRNAs it will need for the next developmental stage. With relatively few known specific transcription factors (ApiAP2 family) that may specifically initiate gene transcription, Plasmodium parasites also regulate the stability and turnover of transcripts to provide more comprehensive gene regulation. The CAF1/CCR4/NOT complex has been shown in model organisms to be important for not only mRNA degradation, but also translational control through its deadenylases CAF1 and CCR4. However, few proteins that impose translational repression in Plasmodium sexual stages are known, and those that are characterized primarily affect female gametocytes. Therefore, we have characterized two deadenylases and have uncovered their roles in transmission. We have identified and characterized CCR4-1, which we show plays a role in activating male gametocytes, stabilizing transcripts in gametocytes, and regulating host-to-vector transmission. We find that when ccr4-1 is genetically deleted, there is a loss in the coordination of male gametocyte activation and a reduction in the ability of the parasite to productively infect the mosquito, which is independent of its effect upon male activation. Comparative RNA-seq shows that the deletion of ccr4-1 affects many transcripts that are translationally repressed in females, are related to male gamete function, and/or are important for early mosquito stage development. In contrast, we found that genetic deletion of the major deadenylase Caf1 is lethal. However, we observed that expression of only the N-terminal Caf1 domain is permissive, yet prevents proper complex assembly and phenocopies the ccr4-1 deletion. We therefore conclude that the general and transmission-specialized deadenylases of the CAF1/CCR4/NOT complex play critical and intertwined roles in parasite growth and transmission.

Dataset Information

An axonemal intron splicing program sustains Plasmodium male development

Publications

An axonemal intron splicing program sustains Plasmodium male development.

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