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

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.

Data availability

Data submitted to SRA, PRJNA503140 : The transcriptome of Guy1-transgenic Anopheles stephensi L1 instar (TaxID: 30069)

The following data sets were generated

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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  1. Yumin Qi
  2. Yang Wu
  3. Randy Saunders
  4. Xiaoguang Chen
  5. Chunhong Mao
  6. James Kite Biedler
  7. Zhijian Jake Tu
(2019)
Guy1, a Y-linked embryonic signal, regulates dosage compensation in Anopheles stephensi by increasing X gene expression
eLife 8:e43570.
https://doi.org/10.7554/eLife.43570

Further reading

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    Research Article Updated

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