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A synthetic sex ratio distortion system for the control of the human malaria mosquito

Author

Listed:
  • Roberto Galizi

    (Imperial College London, South Kensington Campus
    Centro di Genomica Funzionale, University of Perugia, Edificio D)

  • Lindsey A. Doyle

    (Fred Hutchinson Cancer Research Center)

  • Miriam Menichelli

    (Imperial College London, South Kensington Campus)

  • Federica Bernardini

    (Imperial College London, South Kensington Campus)

  • Anne Deredec

    (Imperial College London, South Kensington Campus)

  • Austin Burt

    (Imperial College London, South Kensington Campus)

  • Barry L. Stoddard

    (Fred Hutchinson Cancer Research Center)

  • Nikolai Windbichler

    (Imperial College London, South Kensington Campus)

  • Andrea Crisanti

    (Imperial College London, South Kensington Campus
    Centro di Genomica Funzionale, University of Perugia, Edificio D)

Abstract

It has been theorized that inducing extreme reproductive sex ratios could be a method to suppress or eliminate pest populations. Limited knowledge about the genetic makeup and mode of action of naturally occurring sex distorters and the prevalence of co-evolving suppressors has hampered their use for control. Here we generate a synthetic sex distortion system by exploiting the specificity of the homing endonuclease I-PpoI, which is able to selectively cleave ribosomal gene sequences of the malaria vector Anopheles gambiae that are located exclusively on the mosquito’s X chromosome. We combine structure-based protein engineering and molecular genetics to restrict the activity of the potentially toxic endonuclease to spermatogenesis. Shredding of the paternal X chromosome prevents it from being transmitted to the next generation, resulting in fully fertile mosquito strains that produce >95% male offspring. We demonstrate that distorter male mosquitoes can efficiently suppress caged wild-type mosquito populations, providing the foundation for a new class of genetic vector control strategies.

Suggested Citation

  • Roberto Galizi & Lindsey A. Doyle & Miriam Menichelli & Federica Bernardini & Anne Deredec & Austin Burt & Barry L. Stoddard & Nikolai Windbichler & Andrea Crisanti, 2014. "A synthetic sex ratio distortion system for the control of the human malaria mosquito," Nature Communications, Nature, vol. 5(1), pages 1-8, September.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms4977
    DOI: 10.1038/ncomms4977
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    Cited by:

    1. Beaghton, P.J. & Burt, Austin, 2022. "Gene drives and population persistence vs elimination: The impact of spatial structure and inbreeding at low density," Theoretical Population Biology, Elsevier, vol. 145(C), pages 109-125.
    2. Angela Meccariello & Shibo Hou & Serafima Davydova & James Daniel Fawcett & Alexandra Siddall & Philip T. Leftwich & Flavia Krsticevic & Philippos Aris Papathanos & Nikolai Windbichler, 2024. "Gene drive and genetic sex conversion in the global agricultural pest Ceratitis capitata," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    3. Sebald A. N. Verkuijl & Estela Gonzalez & Ming Li & Joshua X. D. Ang & Nikolay P. Kandul & Michelle A. E. Anderson & Omar S. Akbari & Michael B. Bonsall & Luke Alphey, 2022. "A CRISPR endonuclease gene drive reveals distinct mechanisms of inheritance bias," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    4. Franck Adama Yao & Abdoul-Azize Millogo & Patric Stephane Epopa & Ace North & Florian Noulin & Koulmaga Dao & Mouhamed Drabo & Charles Guissou & Souleymane Kekele & Moussa Namountougou & Robert Kossiv, 2022. "Mark-release-recapture experiment in Burkina Faso demonstrates reduced fitness and dispersal of genetically-modified sterile malaria mosquitoes," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Beaghton, Andrea & Beaghton, Pantelis John & Burt, Austin, 2016. "Gene drive through a landscape: Reaction–diffusion models of population suppression and elimination by a sex ratio distorter," Theoretical Population Biology, Elsevier, vol. 108(C), pages 51-69.
    6. Daniella An Haber & Yael Arien & Lee Benjamin Lamdan & Yehonathan Alcalay & Chen Zecharia & Flavia Krsticevic & Elad Shmuel Yonah & Rotem Daniel Avraham & Elzbieta Krzywinska & Jaroslaw Krzywinski & E, 2024. "Targeting mosquito X-chromosomes reveals complex transmission dynamics of sex ratio distorting gene drives," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    7. Jie Du & Weizhe Chen & Xihua Jia & Xuejiao Xu & Emily Yang & Ruizhi Zhou & Yuqi Zhang & Matt Metzloff & Philipp W. Messer & Jackson Champer, 2024. "Germline Cas9 promoters with improved performance for homing gene drive," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. Silvia Grilli & Roberto Galizi & Chrysanthi Taxiarchi, 2021. "Genetic Technologies for Sustainable Management of Insect Pests and Disease Vectors," Sustainability, MDPI, vol. 13(10), pages 1-19, May.
    9. Rocco D’Amato & Chrysanthi Taxiarchi & Marco Galardini & Alessandro Trusso & Roxana L. Minuz & Silvia Grilli & Alastair G. T. Somerville & Dammy Shittu & Ahmad S. Khalil & Roberto Galizi & Andrea Cris, 2024. "Anti-CRISPR Anopheles mosquitoes inhibit gene drive spread under challenging behavioural conditions in large cages," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    10. Stephanie Gamez & Duverney Chaverra-Rodriguez & Anna Buchman & Nikolay P. Kandul & Stelia C. Mendez-Sanchez & Jared B. Bennett & Héctor M. Sánchez C. & Ting Yang & Igor Antoshechkin & Jonny E. Duque &, 2021. "Exploiting a Y chromosome-linked Cas9 for sex selection and gene drive," Nature Communications, Nature, vol. 12(1), pages 1-14, December.

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