Maternal loss of miRNAs leads to increased variance in primordial germ cell numbers in Drosophila melanogaster

Abstract

MicroRNAs (miRNAs) are posttranscriptional regulators of gene expression that may act as buffering agents to stabilize gene-regulatory networks. Here, we identify two miRNAs that are maternally required for normal embryonic primordial germ cell development in Drosophila melanogaster. Embryos derived from miR-969 and miR-9c mutant mothers had, on average, reduced germ cell numbers. Intriguingly, this reduction correlated with an increase in the variance of this quantitative phenotypic trait. Analysis of an independent set of maternal mutant genotypes suggests that reduction of germ cell number need not lead to increased variance. Our observations are consistent with the hypothesis that miR-969 and miR-9c contribute to stabilizing the processes that control germ number, supporting phenotypic robustness.

Keywords: microRNA; phenotypic trait variance; primordial germ cell development.

Figure 1

Maternal loss of miR-969 and miR-9c leads to reduced primordial germs cell (PGC) numbers. (A) A wild-type embryo at developmental stage S10. PGCs are labeled with α-Vasa (yellow). At S10, PGCs are spread out dorsally toward the embryo surface. (B) Average PGCs numbers in two different laboratory control strains (± SD). (C) Average PGC numbers in embryos derived from miR-969 mutant mothers are reduced in comparison with control and rescued embryos. Error bars correspond to the SD (± SD). Genotypes are (a) Df(1)BSC352/miR-969^KI;;T-969@Fb/+, (b) Df(1)BSC352/miR-969^KI, and (c) Df(1)BSC352/+. (D) Average PGC numbers in embryos derived from miR-9c mutant mothers are reduced in comparison with control and rescued embryos. Genotypes are (d) miR-9c^KO/miR-9c^KO;T-9c@Fb/+, (e) miR-9c^KO/miR-9c^KO;+/nosGal4, (f) miR-9c^KO/miR-9c^KO;T-9c@Fb/nosGal4, (g) miR-9c^KO/+;T-9c@Fb/+, and (h) +/miR-9c^KO;+/nosGal4

Figure 2

Maternal loss of miR-969 and miR-9c leads to elevated primordial germs cell (PGC) number variance. (A) Average PGC number variance is elevated in embryos derived from miR-969 mutant mothers in comparison with control and rescued embryos. Genotypes are (a) Df(1)BSC352/miR-969^KI;;T-969@Fb/+, (b) Df(1)BSC352/miR-969^KI, and (c) Df(1)BSC352/+. (B) Average PGC number variance is elevated in embryos derived from miR-9c mutant mothers in comparison with control and rescued embryos: (d) miR-9c^KO/miR-9c^KO;T-9c@Fb/+, (e) miR-9c^KO/miR-9c^KO;+/nosGal4, (f) miR-9c^KO/miR-9c^KO;T-9c@Fb/nosGal4, (g) miR-9c^KO/+;T-9c@Fb/+, and (h) +/miR-9c^KO;+/nosGal4. (C) Increased PGC number variance (y-axis) does not generally increase with reduced PGC numbers (x-axis). Data points were originally published in Kugler et al. 2010.