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EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis

Author

Listed:
  • Shuzhen Yang

    (Xiamen University)

  • Mengya Cai

    (Xiamen University)

  • Junjie Huang

    (Wuhan University)

  • Shengnan Zhang

    (Xiamen University)

  • Xiaoli Mo

    (Xiamen University)

  • Kai Jiang

    (Wuhan University
    Wuhan University)

  • Huiting Cui

    (Xiamen University)

  • Jing Yuan

    (Xiamen University)

Abstract

Faithful chromosome segregation of 8 duplicated haploid genomes into 8 daughter gametes is essential for male gametogenesis and mosquito transmission of Plasmodium. Plasmodium undergoes endomitosis in this multinucleated cell division, which is highly reliant on proper spindle-kinetochore attachment. However, the mechanisms underlying the spindle-kinetochore attachment remain elusive. End-binding proteins (EBs) are conserved microtubule (MT) plus-end binding proteins and play an important role in regulating MT plus-end dynamics. Here, we report that the Plasmodium EB1 is an orthologue distinct from the canonical eukaryotic EB1. Both in vitro and in vivo assays reveal that the Plasmodium EB1 losses MT plus-end tracking but possesses MT-lattice affinity. This MT-binding feature of Plasmodium EB1 is contributed by both CH domain and linker region. EB1-deficient parasites produce male gametocytes that develop to the anucleated male gametes, leading to defective mosquito transmission. EB1 is localized at the nucleoplasm of male gametocytes. During the gametogenesis, EB1 decorates the full-length of spindle MTs and regulates spindle structure. The kinetochores attach to spindle MTs laterally throughout endomitosis and this attachment is EB1-dependent. Consequently, impaired spindle-kinetochore attachment is observed in EB1-deficient parasites. These results indicate that a parasite-specific EB1 with MT-lattice binding affinity fulfills the spindle-kinetochore lateral attachment in male gametogenesis.

Suggested Citation

  • Shuzhen Yang & Mengya Cai & Junjie Huang & Shengnan Zhang & Xiaoli Mo & Kai Jiang & Huiting Cui & Jing Yuan, 2023. "EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38516-3
    DOI: 10.1038/s41467-023-38516-3
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    References listed on IDEAS

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    1. Jiahong Li & Gerald J. Shami & Ellie Cho & Boyin Liu & Eric Hanssen & Matthew W. A. Dixon & Leann Tilley, 2022. "Repurposing the mitotic machinery to drive cellular elongation and chromatin reorganisation in Plasmodium falciparum gametocytes," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Roshan L. Shrestha & Duccio Conti & Naoka Tamura & Dominique Braun & Revathy A. Ramalingam & Konstanty Cieslinski & Jonas Ries & Viji M. Draviam, 2017. "Aurora-B kinase pathway controls the lateral to end-on conversion of kinetochore-microtubule attachments in human cells," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
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    1. Mohammad Zeeshan & Edward Rea & Steven Abel & Kruno Vukušić & Robert Markus & Declan Brady & Antonius Eze & Ravish Rashpa & Aurelia C. Balestra & Andrew R. Bottrill & Mathieu Brochet & David S. Gutter, 2023. "Plasmodium ARK2 and EB1 drive unconventional spindle dynamics, during chromosome segregation in sexual transmission stages," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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