A new component of the Nasonia sex determining cascade is maternally silenced and regulates transformer expression

PLoS One. 2013 May 22;8(5):e63618. doi: 10.1371/journal.pone.0063618. Print 2013.

Abstract

Although sex determination is a universal process in sexually reproducing organisms, sex determination pathways are among the most highly variable genetic systems found in nature. Nevertheless, general principles can be identified among the diversity, like the central role of transformer (tra) in insects. When a functional TRA protein is produced in early embryogenesis, the female sex determining route is activated, while prevention of TRA production leads to male development. In dipterans, male development is achieved by prevention of female-specific splicing of tra mRNA, either mediated by X-chromosome dose or masculinizing factors. In Hymenoptera, which have haplodiploid sex determination, complementary sex determination and maternal imprinting have been identified to regulate timely TRA production. In the parasitoid Nasonia, zygotic transformer (Nvtra) expression and splicing is regulated by a combination of maternal provision of Nvtra mRNA and silencing of Nvtra expression in unfertilized eggs. It is unclear, however, if this silencing is directly on the tra locus or whether it is mediated through maternal silencing of a trans-acting factor. Here we show that in Nasonia, female sex determination is dependent on zygotic activation of Nvtra expression by an as yet unknown factor. This factor, which we propose to term womanizer (wom), is maternally silenced during oogenesis to ensure male development in unfertilized eggs. This finding implicates the upstream recruitment of a novel gene in the Nasonia sex determining cascade and supports the notion that sex determining cascades can rapidly change by adding new components on top of existing regulators.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • Female
  • Gene Expression Regulation, Developmental / genetics*
  • Insect Proteins / genetics*
  • Insect Proteins / metabolism
  • Male
  • Ovum / metabolism
  • Sex Determination Processes / genetics*
  • Wasps / genetics*
  • Wasps / metabolism
  • Zygote / metabolism

Substances

  • Insect Proteins

Grant support

Eveline C. Verhulst was supported by NWO ALW TOP grant no.∼854.10.001 granted to Leo W. Beukeboom and Louis van de Zande (http://www.nwo.nl/). Jeremy A. Lynch was funded by the SFB 680 “Molecular Basis of Evolutionary Innovations”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.