EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis
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 a...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-05-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-38516-3 |
| _version_ | 1797822767195750400 |
|---|---|
| author | Shuzhen Yang Mengya Cai Junjie Huang Shengnan Zhang Xiaoli Mo Kai Jiang Huiting Cui Jing Yuan |
| author_facet | Shuzhen Yang Mengya Cai Junjie Huang Shengnan Zhang Xiaoli Mo Kai Jiang Huiting Cui Jing Yuan |
| author_sort | Shuzhen Yang |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-13T10:14:01Z |
| format | Article |
| id | doaj.art-dcb318fb549b4eb893ba8889c3778a82 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-13T10:14:01Z |
| publishDate | 2023-05-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-dcb318fb549b4eb893ba8889c3778a822023-05-21T11:21:02ZengNature PortfolioNature Communications2041-17232023-05-0114112010.1038/s41467-023-38516-3EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesisShuzhen Yang0Mengya Cai1Junjie Huang2Shengnan Zhang3Xiaoli Mo4Kai Jiang5Huiting Cui6Jing Yuan7State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Faculty of Medicine and Life Sciences, Xiamen UniversityState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Faculty of Medicine and Life Sciences, Xiamen UniversityThe State Key Laboratory Breeding Base of Basic Science of Stomatology and Key Laboratory of Oral Biomedicine Ministry of Education, School & Hospital of Stomatology, Medical Research Institute, Wuhan UniversityState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Faculty of Medicine and Life Sciences, Xiamen UniversityState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Faculty of Medicine and Life Sciences, Xiamen UniversityThe State Key Laboratory Breeding Base of Basic Science of Stomatology and Key Laboratory of Oral Biomedicine Ministry of Education, School & Hospital of Stomatology, Medical Research Institute, Wuhan UniversityState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Faculty of Medicine and Life Sciences, Xiamen UniversityState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Faculty of Medicine and Life Sciences, Xiamen UniversityAbstract 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.https://doi.org/10.1038/s41467-023-38516-3 |
| spellingShingle | Shuzhen Yang Mengya Cai Junjie Huang Shengnan Zhang Xiaoli Mo Kai Jiang Huiting Cui Jing Yuan EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis Nature Communications |
| title | EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis |
| title_full | EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis |
| title_fullStr | EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis |
| title_full_unstemmed | EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis |
| title_short | EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis |
| title_sort | eb1 decoration of microtubule lattice facilitates spindle kinetochore lateral attachment in plasmodium male gametogenesis |
| url | https://doi.org/10.1038/s41467-023-38516-3 |
| work_keys_str_mv | AT shuzhenyang eb1decorationofmicrotubulelatticefacilitatesspindlekinetochorelateralattachmentinplasmodiummalegametogenesis AT mengyacai eb1decorationofmicrotubulelatticefacilitatesspindlekinetochorelateralattachmentinplasmodiummalegametogenesis AT junjiehuang eb1decorationofmicrotubulelatticefacilitatesspindlekinetochorelateralattachmentinplasmodiummalegametogenesis AT shengnanzhang eb1decorationofmicrotubulelatticefacilitatesspindlekinetochorelateralattachmentinplasmodiummalegametogenesis AT xiaolimo eb1decorationofmicrotubulelatticefacilitatesspindlekinetochorelateralattachmentinplasmodiummalegametogenesis AT kaijiang eb1decorationofmicrotubulelatticefacilitatesspindlekinetochorelateralattachmentinplasmodiummalegametogenesis AT huitingcui eb1decorationofmicrotubulelatticefacilitatesspindlekinetochorelateralattachmentinplasmodiummalegametogenesis AT jingyuan eb1decorationofmicrotubulelatticefacilitatesspindlekinetochorelateralattachmentinplasmodiummalegametogenesis |