A novel SUN1-ALLAN complex coordinates segregation of the bipartite MTOC across the nuclear envelope during rapid closed mitosis in Plasmodium berghei
Mitosis in eukaryotes involves reorganisation of the nuclear envelope (NE) and microtubule-organising centres (MTOCs). During male gametogenesis in Plasmodium , the causative agent of malaria, mitosis is exceptionally rapid and highly divergent. Within 8 min, the haploid male gametocyte genome undergoes three replication cycles (1N to 8N), while maintaining an intact NE. Axonemes assemble in the cytoplasm and connect to a bipartite MTOC-containing nuclear pole (NP) and cytoplasmic basal body, producing eight flagellated gametes. The mechanisms coordinating NE remodelling, MTOC dynamics, and flagellum assembly remain poorly understood. We identify the SUN1-ALLAN complex as a novel mediator of NE remodelling and bipartite MTOC coordination during Plasmodium berghei male gametogenesis. SUN1, a conserved NE protein, localises to dynamic loops and focal points at the nucleoplasmic face of the spindle poles. ALLAN, a divergent allantoicase, has a location like that of SUN1, and these proteins form a unique complex, detected by live-cell imaging, ultrastructural expansion microscopy, and interactomics. Deletion of either SUN1 or ALLAN genes disrupts nuclear MTOC organisation, leading to basal body mis-segregation, defective spindle assembly, and impaired spindle microtubule-kinetochore attachment, but axoneme formation remains intact. Ultrastructural analysis revealed nuclear and cytoplasmic MTOC miscoordination, producing aberrant flagellated gametes lacking nuclear material. These defects block development in the mosquito and parasite transmission, highlighting the essential functions of this complex.
Authors
- Zeinab Chahine (ORCID: https://orcid.org/0000-0001-8208-5869)
- Declan Brady (ORCID: https://orcid.org/0000-0001-9150-7840)
- Andrew R. Bottrill (ORCID: https://orcid.org/0000-0002-5182-3643)
- Cyrille Y. Botté (ORCID: https://orcid.org/0000-0002-2245-536X)
- Karine G. Le Roch (ORCID: https://orcid.org/0000-0002-4862-9292)
- Akancha Mishra (ORCID: https://orcid.org/0009-0005-4775-3338)
- Róbert Márkus (ORCID: https://orcid.org/0000-0003-4535-303X)
- Igor Blatov (ORCID: https://orcid.org/0000-0003-2110-0441)
- Eelco C. Tromer (ORCID: https://orcid.org/0000-0003-3540-7727)
- Mohammad Zeeshan (ORCID: https://orcid.org/0000-0002-6185-403X)
- Ryuji Yanase (ORCID: https://orcid.org/0000-0001-9419-398X)
- Rita Tewari (ORCID: https://orcid.org/0000-0003-3943-1847)
- Sagar Batra (ORCID: https://orcid.org/0000-0003-3986-5047)
- Sarah L. Pashley (ORCID: https://orcid.org/0000-0002-9948-1777)
- David Ferguson (ORCID: https://orcid.org/0000-0001-5045-819X)
- Anthony A. Holder (ORCID: https://orcid.org/0000-0002-8490-6058)
- Sue Vaughan (ORCID: https://orcid.org/0000-0002-0925-4491)
- Yoshiki Yamaryo‐Botté (ORCID: https://orcid.org/0000-0002-9349-4411)
- Molly Hair (ORCID: https://orcid.org/0009-0005-9352-9900)
- Suhani Bhanvadia
- Baptiste Marché
Institutions
- University of California, Riverside (US)
- Oxford Brookes University (GB)
- Centre National de la Recherche Scientifique (FR)
- Biotechnology Institute (US)
- University of Nottingham (GB)
- University of Groningen (NL)
- The Francis Crick Institute (GB)
- University of Warwick (GB)
- Université Grenoble Alpes (FR)
Publication Details
- Journal
- eLife
- Published
- 2025-05-20
- DOI
- https://doi.org/10.7554/elife.106537.2
- Citations
- 2
- Primary Topic
- Nuclear Structure and Function
- Type
- article
- Field-Weighted Citation Impact
- 1.61
Funders
- Francis Crick Institute
- Agence Nationale de la Recherche
- Indo-French Centre for the Promotion of Advanced Research
- Fondation pour la Recherche Médicale
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- The Wellcome Trust DBT India Alliance
- University of California, Riverside
- Biotechnology and Biological Sciences Research Council
- National Institute of Allergy and Infectious Diseases