Abstract
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.
Highlights
Insects employ diverse sex-determination mechanisms at the chromosomal level including XX/XY, ZW/ZZ, XX/XO, and diploid/haploid chromosomal systems (Bopp et al, 2014; Bachtrog et al, 2014; Biedler and Tu, 2016)
We have previously shown that Guy1 is the earliest expressed Y chromosome gene and it is transcribed at the onset of maternal-to-zygotic transition, prior to sex-determination (Criscione et al, 2013)
We have shown in transgenic lines that the native Guy1 promoter is able to direct Guy1 transcription as well as GUY1 function when placed in the autosome of genetic females which lack the Y chromosome
Summary
Insects employ diverse sex-determination mechanisms at the chromosomal level including XX/XY, ZW/ZZ, XX/XO, and diploid/haploid chromosomal systems (Bopp et al, 2014; Bachtrog et al, 2014; Biedler and Tu, 2016). In honeybees which use the diploid/haploid system, heterozygosity of the complementary sex determiner (csd) gene is the primary signal that initiates female development ( Hasselmann et al, 2008). A dominant male-determining factor (M) on the Y chromosome initiates male development in many other insects that contain XX/XY sex chromosomes (Sanchez, 2008; Biedler and Tu, 2016). Instead of a well differentiated and heteromorphic Y chromosome, mosquitoes of the Culicinae subfamily, which includes the genus Aedes, contain a homomorphic sex-determining chromosome that harbors an M factor in the male-determining locus (M-locus). A novel RNA-binding protein named Nix was recently shown to be an M factor in Aedes aegypti (Hall et al, 2015)
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