1. Developmental Biology
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Guy1, a Y-linked embryonic signal, regulates dosage compensation in Anopheles stephensi by increasing X gene expression

  1. Yumin Qi
  2. Yang Wu
  3. Randy Saunders
  4. Xiaoguang Chen
  5. Chunhong Mao
  6. James Kite Biedler  Is a corresponding author
  7. Zhijian Jake Tu  Is a corresponding author
  1. Virginia Tech, United States
  2. Southern Medical University, China
  3. Virginia Biocomplexity Institute, United States
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Cite this article as: eLife 2019;8:e43570 doi: 10.7554/eLife.43570

Abstract

We previously showed that Guy1, a primary signal expressed from the Y chromosome, is a strong candidate for a male-determining factor that confers female-specific lethality in Anopheles stephensi (Criscione et al., 2016). Here we present evidence that Guy1 increases X gene expression in Guy1-transgenic females from two independent lines, providing a mechanism underlying the Guy1-conferred female lethality. The median level gene expression (MGE) of X-linked genes is significantly higher than autosomal genes in Guy1-transgenic females while there is no significant difference in MGE between X and autosomal genes in wild type females. Furthermore, Guy1 significantly up-regulates at least 40% of the 996 genes across the X chromosome in transgenic females. Guy1-conferred female-specific lethality is remarkably stable and completely penetrant. These findings indicate that Guy1 regulates dosage compensation in An. stephensi and components of dosage compensation may be explored to develop novel strategies to control mosquito-borne diseases.

Article and author information

Author details

  1. Yumin Qi

    Department of Biochemistry, Virginia Tech, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Yang Wu

    Department of Pathogen Biology, School of Public Health, Southern Medical University, Guangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1207-5566

  3. Randy Saunders

    Department of Biochemistry, Virginia Tech, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Xiaoguang Chen

    Department of Pathogen Biology, School of Public Health, Southern Medical University, Guangzhou, China
    Competing interests
    The authors declare that no competing interests exist.

  5. Chunhong Mao

    Virginia Biocomplexity Institute, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. James Kite Biedler

    Department of Biochemistry, Virginia Tech, Blacksburg, United States
    For correspondence
    jbiedler@vt.edu
    Competing interests
    The authors declare that no competing interests exist.

  7. Zhijian Jake Tu

    Department of Biochemistry, Virginia Tech, Blacksburg, United States
    For correspondence
    jaketu@vt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4227-3819

Funding

National Institutes of Health (AI105575)

  • Zhijian Jake Tu

National Institutes of Health (AI121284)

  • Zhijian Jake Tu

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (IACUC #16-067) of the Virginia Tech.

Reviewing Editor

  1. Yukiko M Yamashita, University of Michigan, United States

Publication history

  1. Received: November 16, 2018
  2. Accepted: March 16, 2019
  3. Accepted Manuscript published: March 19, 2019 (version 1)
  4. Version of Record published: March 29, 2019 (version 2)

Copyright

© 2019, Qi et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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Further reading

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    2. Microbiology and Infectious Disease

    GUY1 confers complete female lethality and is a strong candidate for a male-determining factor in Anopheles stephensi

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    Despite their importance in sexual differentiation and reproduction, Y chromosome genes are rarely described because they reside in repeat-rich regions that are difficult to study. Here, we show that Guy1, a unique Y chromosome gene of a major urban malaria mosquito Anopheles stephensi, confers 100% female lethality when placed on the autosomes. We show that the small GUY1 protein (56 amino acids in length) causes female lethality and that males carrying the transgene are reproductively more competitive than their non-transgenic siblings under laboratory conditions. The GUY1 protein is a primary signal from the Y chromosome that affects embryonic development in a sex-specific manner. Our results have demonstrated, for the first time in mosquitoes, the feasibility of stable transgenic manipulation of sex ratios using an endogenous gene from the male-determining chromosome. These results provide insights into the elusive M factor and suggest exciting opportunities to reduce mosquito populations and disease transmission.

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