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Radial spoke protein 9 is necessary for axoneme assembly in Plasmodium but not in trypanosomatid parasites
Flagella are important for eukaryote cell motility, including in sperm, and are vital for life cycle progression of many unicellular eukaryotic pathogens. The ‘9+2’ axoneme in most motile flagella comprises nine outer doublet and two central-pair singlet microtubules. T-shaped radial spokes protrude...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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The Company of Biologists Ltd
2023
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10309588/ https://www.ncbi.nlm.nih.gov/pubmed/37288670 http://dx.doi.org/10.1242/jcs.260655 |
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author | Ramakrishnan, Chandra Fort, Cécile Marques, Sara Rute Ferguson, David J. P. Gransagne, Marion Baum, Jake Chaouch, Soraya Mouray, Elisabeth Kohl, Linda Wheeler, Richard J. Sinden, Robert E. |
author_facet | Ramakrishnan, Chandra Fort, Cécile Marques, Sara Rute Ferguson, David J. P. Gransagne, Marion Baum, Jake Chaouch, Soraya Mouray, Elisabeth Kohl, Linda Wheeler, Richard J. Sinden, Robert E. |
author_sort | Ramakrishnan, Chandra |
collection | PubMed |
description | Flagella are important for eukaryote cell motility, including in sperm, and are vital for life cycle progression of many unicellular eukaryotic pathogens. The ‘9+2’ axoneme in most motile flagella comprises nine outer doublet and two central-pair singlet microtubules. T-shaped radial spokes protrude from the outer doublets towards the central pair and are necessary for effective beating. We asked whether there were radial spoke adaptations associated with parasite lineage-specific properties in apicomplexans and trypanosomatids. Following an orthologue search for experimentally uncharacterised radial spoke proteins (RSPs), we identified and analysed RSP9. Trypanosoma brucei and Leishmania mexicana have an extensive RSP complement, including two divergent RSP9 orthologues, necessary for flagellar beating and swimming. Detailed structural analysis showed that neither orthologue is needed for axoneme assembly in Leishmania. In contrast, Plasmodium has a reduced set of RSPs including a single RSP9 orthologue, deletion of which in Plasmodium berghei leads to failure of axoneme formation, failed male gamete release, greatly reduced fertilisation and inefficient life cycle progression in the mosquito. This indicates contrasting selection pressures on axoneme complexity, likely linked to the different mode of assembly of trypanosomatid versus Plasmodium flagella. |
format | Online Article Text |
id | pubmed-10309588 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | The Company of Biologists Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-103095882023-06-30 Radial spoke protein 9 is necessary for axoneme assembly in Plasmodium but not in trypanosomatid parasites Ramakrishnan, Chandra Fort, Cécile Marques, Sara Rute Ferguson, David J. P. Gransagne, Marion Baum, Jake Chaouch, Soraya Mouray, Elisabeth Kohl, Linda Wheeler, Richard J. Sinden, Robert E. J Cell Sci Research Article Flagella are important for eukaryote cell motility, including in sperm, and are vital for life cycle progression of many unicellular eukaryotic pathogens. The ‘9+2’ axoneme in most motile flagella comprises nine outer doublet and two central-pair singlet microtubules. T-shaped radial spokes protrude from the outer doublets towards the central pair and are necessary for effective beating. We asked whether there were radial spoke adaptations associated with parasite lineage-specific properties in apicomplexans and trypanosomatids. Following an orthologue search for experimentally uncharacterised radial spoke proteins (RSPs), we identified and analysed RSP9. Trypanosoma brucei and Leishmania mexicana have an extensive RSP complement, including two divergent RSP9 orthologues, necessary for flagellar beating and swimming. Detailed structural analysis showed that neither orthologue is needed for axoneme assembly in Leishmania. In contrast, Plasmodium has a reduced set of RSPs including a single RSP9 orthologue, deletion of which in Plasmodium berghei leads to failure of axoneme formation, failed male gamete release, greatly reduced fertilisation and inefficient life cycle progression in the mosquito. This indicates contrasting selection pressures on axoneme complexity, likely linked to the different mode of assembly of trypanosomatid versus Plasmodium flagella. The Company of Biologists Ltd 2023-06-08 /pmc/articles/PMC10309588/ /pubmed/37288670 http://dx.doi.org/10.1242/jcs.260655 Text en © 2023. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0 (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. |
spellingShingle | Research Article Ramakrishnan, Chandra Fort, Cécile Marques, Sara Rute Ferguson, David J. P. Gransagne, Marion Baum, Jake Chaouch, Soraya Mouray, Elisabeth Kohl, Linda Wheeler, Richard J. Sinden, Robert E. Radial spoke protein 9 is necessary for axoneme assembly in Plasmodium but not in trypanosomatid parasites |
title | Radial spoke protein 9 is necessary for axoneme assembly in Plasmodium but not in trypanosomatid parasites |
title_full | Radial spoke protein 9 is necessary for axoneme assembly in Plasmodium but not in trypanosomatid parasites |
title_fullStr | Radial spoke protein 9 is necessary for axoneme assembly in Plasmodium but not in trypanosomatid parasites |
title_full_unstemmed | Radial spoke protein 9 is necessary for axoneme assembly in Plasmodium but not in trypanosomatid parasites |
title_short | Radial spoke protein 9 is necessary for axoneme assembly in Plasmodium but not in trypanosomatid parasites |
title_sort | radial spoke protein 9 is necessary for axoneme assembly in plasmodium but not in trypanosomatid parasites |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10309588/ https://www.ncbi.nlm.nih.gov/pubmed/37288670 http://dx.doi.org/10.1242/jcs.260655 |
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