Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila.
In the textbook view, the ratio of X chromosomes to autosome sets, X:A, is the primary signal specifying sexual fate in Drosophila. An alternative idea is that X chromosome number signals sex through the direct actions of several X-encoded signal element (XSE) proteins. In this alternative, the influence of autosome dose on X chromosome counting is largely indirect. Haploids (1X;1A), which possess the male number of X chromosomes but the female X:A of 1.0, and triploid intersexes (XX;AAA), which possess a female dose of two X chromosomes and the ambiguous X:A ratio of 0.67, represent critical tests of these hypotheses. To directly address the effects of ploidy in primary sex determination, we compared the responses of the signal target, the female-specific SxlPe promoter of the switch gene Sex-lethal, in haploid, diploid, and triploid embryos. We found that haploids activate SxlPe because an extra precellular nuclear division elevates total X chromosome numbers and XSE levels beyond those in diploid males. Conversely, triploid embryos cellularize one cycle earlier than diploids, causing premature cessation of SxlPe expression. This prevents XX;AAA embryos from fully engaging the autoregulatory mechanism that maintains subsequent Sxl expression, causing them to develop as sexual mosaics. We conclude that the X:A ratio predicts sexual fate, but does not actively specify it. Instead, the instructive X chromosome signal is more appropriately seen as collective XSE dose in the early embryo. Our findings reiterate that correlations between X:A ratios and cell fates in other organisms need not implicate the value of the ratio as an active signal.
Erickson
James W
JW
Department of Biology, Texas A&M University, College Station, Texas, United States of America. jerickson@mail.bio.tamu.edu
Quintero
Jerome J
JJ
D000818:Animals; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster / Q000235:genetics* / Q000378:metabolism; D004625:Embryo, Nonmammalian / Q000196:embryology / Q000378:metabolism; D005260:Female; D018628:Gene Dosage / Q000235:genetics*; D018507:Gene Expression Regulation, Developmental; D008297:Male; D008954:Models, Biological; D010641:Phenotype; D011003:Ploidies; D016601:RNA-Binding Proteins / Q000235:genetics / Q000378:metabolism; D012730:Sex Chromosomes / Q000235:genetics*; D019849:Sex Determination Processes; D013997:Time Factors; D014158:Transcription, Genetic / Q000235:genetics
D029721:Drosophila Proteins; D016601:RNA-Binding Proteins; C067777:Sxl protein, Drosophila