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Regulators of male and female sexual development critical for transmission of a malaria parasite

View ORCID ProfileAndrew J C Russell, View ORCID ProfileTheo Sanderson, View ORCID ProfileEllen Bushell, View ORCID ProfileArthur M Talman, Burcu Anar, View ORCID ProfileGareth Girling, View ORCID ProfileMirjam Hunziker, View ORCID ProfileRobyn S Kent, Tom Metcalf, Ruddy Montandon, Vikash Pandey, A Brett Roberts, View ORCID ProfileClaire Sayers, View ORCID ProfileFrank Schwach, View ORCID ProfileJulian C Rayner, View ORCID ProfileThierry Voet, View ORCID ProfileKatarzyna K Modrzynska, View ORCID ProfileAndrew P. Waters, View ORCID ProfileMara K N Lawniczak, View ORCID ProfileOliver Billker
doi: https://doi.org/10.1101/2021.08.04.455056
Andrew J C Russell
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
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Theo Sanderson
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
2Francis Crick Institute, 1 Midland Road, London NW1 1AT, United Kingdom
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Ellen Bushell
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
3Laboratory for Molecular Infection Medicine Sweden, Umeå University, Umeå S-90187, Sweden
4Department of Molecular Biology, Umeå University, Umeå S-90187, Sweden
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Arthur M Talman
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
5MIVEGEC, University of Montpellier, IRD, CNRS, Montpellier, France
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Burcu Anar
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
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Gareth Girling
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
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Mirjam Hunziker
3Laboratory for Molecular Infection Medicine Sweden, Umeå University, Umeå S-90187, Sweden
4Department of Molecular Biology, Umeå University, Umeå S-90187, Sweden
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Robyn S Kent
6Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, G12 8TA, United Kingdom
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Tom Metcalf
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
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Ruddy Montandon
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
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Vikash Pandey
3Laboratory for Molecular Infection Medicine Sweden, Umeå University, Umeå S-90187, Sweden
4Department of Molecular Biology, Umeå University, Umeå S-90187, Sweden
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A Brett Roberts
6Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, G12 8TA, United Kingdom
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Claire Sayers
3Laboratory for Molecular Infection Medicine Sweden, Umeå University, Umeå S-90187, Sweden
4Department of Molecular Biology, Umeå University, Umeå S-90187, Sweden
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Frank Schwach
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
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Julian C Rayner
7Cambridge Institute for Medical Research, University of Cambridge, Cambridge CB2 0XY, United Kingdom
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Thierry Voet
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
8Department of Human Genetics, University of Leuven, KU Leuven, Leuven, Belgium
9KU Leuven Institute for Single Cell Omics, LISCO, KU Leuven, Leuven, Belgium
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Katarzyna K Modrzynska
6Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, G12 8TA, United Kingdom
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Andrew P. Waters
6Wellcome Centre for Integrative Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, G12 8TA, United Kingdom
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  • For correspondence: andy.waters@glasgow.ac.uk mara@sanger.ac.uk oliver.billker@umu.se
Mara K N Lawniczak
1Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
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  • For correspondence: andy.waters@glasgow.ac.uk mara@sanger.ac.uk oliver.billker@umu.se
Oliver Billker
3Laboratory for Molecular Infection Medicine Sweden, Umeå University, Umeå S-90187, Sweden
4Department of Molecular Biology, Umeå University, Umeå S-90187, Sweden
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  • For correspondence: andy.waters@glasgow.ac.uk mara@sanger.ac.uk oliver.billker@umu.se
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Summary

The transmission of malaria parasites from vertebrate host to mosquito vector requires a developmental switch in asexually dividing blood-stage parasites to sexual reproduction. In Plasmodium berghei the transcription factor AP2-G is required and sufficient for this switch, but how a particular sex is determined in a haploid parasite remains unknown. Using a global screen of barcoded mutants, we here identify ten genes essential for the formation of either male or female sexual forms and validate their importance for transmission. High-resolution single-cell transcriptomics of wild-type and mutant parasites portrays the developmental bifurcation and reveals a regulatory cascade of putative gene functions in determination and subsequent differentiation of each sex. A male-determining gene with a LOTUS/OST-HTH domain points towards unexpected conservation of molecular mechanisms of gametogenesis in animals and a distantly related eukaryotic parasite.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://www.ebi.ac.uk/ena/browser/view/PRJEB44892

  • https://plasmogem.shinyapps.io/Gametocytes_Shiny/

  • https://www.malariacellatlas.org

  • http://obilab.molbiol.umu.se/gcsko

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted August 04, 2021.
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Regulators of male and female sexual development critical for transmission of a malaria parasite
Andrew J C Russell, Theo Sanderson, Ellen Bushell, Arthur M Talman, Burcu Anar, Gareth Girling, Mirjam Hunziker, Robyn S Kent, Tom Metcalf, Ruddy Montandon, Vikash Pandey, A Brett Roberts, Claire Sayers, Frank Schwach, Julian C Rayner, Thierry Voet, Katarzyna K Modrzynska, Andrew P. Waters, Mara K N Lawniczak, Oliver Billker
bioRxiv 2021.08.04.455056; doi: https://doi.org/10.1101/2021.08.04.455056
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Regulators of male and female sexual development critical for transmission of a malaria parasite
Andrew J C Russell, Theo Sanderson, Ellen Bushell, Arthur M Talman, Burcu Anar, Gareth Girling, Mirjam Hunziker, Robyn S Kent, Tom Metcalf, Ruddy Montandon, Vikash Pandey, A Brett Roberts, Claire Sayers, Frank Schwach, Julian C Rayner, Thierry Voet, Katarzyna K Modrzynska, Andrew P. Waters, Mara K N Lawniczak, Oliver Billker
bioRxiv 2021.08.04.455056; doi: https://doi.org/10.1101/2021.08.04.455056

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