IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-49002-9.html
   My bibliography  Save this article

An axonemal intron splicing program sustains Plasmodium male development

Author

Listed:
  • 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
    Xiamen University)

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.

Suggested Citation

  • Jiepeng Guan & Peijia Wu & Xiaoli Mo & Xiaolong Zhang & Wenqi Liang & Xiaoming Zhang & Lubin Jiang & Jian Li & Huiting Cui & Jing Yuan, 2024. "An axonemal intron splicing program sustains Plasmodium male development," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49002-9
    DOI: 10.1038/s41467-024-49002-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-49002-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-49002-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Miho Usui & Surendra K. Prajapati & Ruth Ayanful-Torgby & Festus K. Acquah & Elizabeth Cudjoe & Courage Kakaney & Jones A. Amponsah & Evans K. Obboh & Deepti K. Reddy & Michelle C. Barbeau & Lacy M. S, 2019. "Plasmodium falciparum sexual differentiation in malaria patients is associated with host factors and GDV1-dependent genes," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    2. O. Billker & V. Lindo & M. Panico & A. E. Etienne & T. Paxton & A. Dell & M. Rogers & R. E. Sinden & H. R. Morris, 1998. "Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito," Nature, Nature, vol. 392(6673), pages 289-292, March.
    3. Tianyang Liu & Fiona Shilliday & Alexander D. Cook & Mohammad Zeeshan & Declan Brady & Rita Tewari & Colin J. Sutherland & Anthony J. Roberts & Carolyn A. Moores, 2022. "Mechanochemical tuning of a kinesin motor essential for malaria parasite transmission," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Yuanyuan Jiang & Jun Wei & Huiting Cui & Chuanyuan Liu & Yuan Zhi & ZhengZheng Jiang & Zhenkui Li & Shaoneng Li & Zhenke Yang & Xu Wang & Pengge Qian & Cui Zhang & Chuanqi Zhong & Xin-zhuan Su & Jing , 2020. "An intracellular membrane protein GEP1 regulates xanthurenic acid induced gametogenesis of malaria parasites," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    5. Gabrielle A. Josling & Timothy J. Russell & Jarrett Venezia & Lindsey Orchard & Riëtte Biljon & Heather J. Painter & Manuel Llinás, 2020. "Dissecting the role of PfAP2-G in malaria gametocytogenesis," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    6. Miho Usui & Surendra K. Prajapati & Ruth Ayanful-Torgby & Festus K. Acquah & Elizabeth Cudjoe & Courage Kakaney & Jones A. Amponsah & Evans K. Obboh & Deepti K. Reddy & Michelle C. Barbeau & Lacy M. S, 2019. "Publisher Correction: Plasmodium falciparum sexual differentiation in malaria patients is associated with host factors and GDV1-dependent genes," Nature Communications, Nature, vol. 10(1), pages 1-1, December.
    7. Abhinav Sinha & Katie R. Hughes & Katarzyna K. Modrzynska & Thomas D. Otto & Claudia Pfander & Nicholas J. Dickens & Agnieszka A. Religa & Ellen Bushell & Anne L. Graham & Rachael Cameron & Bjorn F. C, 2014. "A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium," Nature, Nature, vol. 507(7491), pages 253-257, March.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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 &, 2023. "Novel insights into the role of long non-coding RNA in the human malaria parasite, Plasmodium falciparum," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Bing Guo & Victor Borda & Roland Laboulaye & Michele D. Spring & Mariusz Wojnarski & Brian A. Vesely & Joana C. Silva & Norman C. Waters & Timothy D. O’Connor & Shannon Takala-Harrison, 2024. "Strong positive selection biases identity-by-descent-based inferences of recent demography and population structure in Plasmodium falciparum," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Jin-Lei Wang & Ting-Ting Li & Nian-Zhang Zhang & Meng Wang & Li-Xiu Sun & Zhi-Wei Zhang & Bao-Quan Fu & Hany M. Elsheikha & Xing-Quan Zhu, 2024. "The transcription factor AP2XI-2 is a key negative regulator of Toxoplasma gondii merogony," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Ravish Rashpa & Natacha Klages & Domitille Schvartz & Carla Pasquarello & Mathieu Brochet, 2023. "The Skp1-Cullin1-FBXO1 complex is a pleiotropic regulator required for the formation of gametes and motile forms in Plasmodium berghei," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Brittany Hazzard & Juliana M. Sá & Haikel N. Bogale & Tales V. Pascini & Angela C. Ellis & Shuchi Amin & Jennifer S. Armistead & John H. Adams & Thomas E. Wellems & David Serre, 2024. "Single-cell analyses of polyclonal Plasmodium vivax infections and their consequences on parasite transmission," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49002-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.