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

Kugler JM, Chen YW, Weng R, Cohen SM - G3 (Bethesda) (2013)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Molecular and Cell Biology, Singapore 138673, Republic of Singapore.

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.

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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-969KI;;T-969@Fb/+, (b) Df(1)BSC352/miR-969KI, 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-9cKO/miR-9cKO;T-9c@Fb/+, (e) miR-9cKO/miR-9cKO;+/nosGal4, (f) miR-9cKO/miR-9cKO;T-9c@Fb/nosGal4, (g) miR-9cKO/+;T-9c@Fb/+, and (h) +/miR-9cKO;+/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.
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fig2: 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-969KI;;T-969@Fb/+, (b) Df(1)BSC352/miR-969KI, 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-9cKO/miR-9cKO;T-9c@Fb/+, (e) miR-9cKO/miR-9cKO;+/nosGal4, (f) miR-9cKO/miR-9cKO;T-9c@Fb/nosGal4, (g) miR-9cKO/+;T-9c@Fb/+, and (h) +/miR-9cKO;+/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.

Mentions: In addition, we noted that the range of PGC numbers was broader in embryos from the miRNA mutant mothers than from the controls. Some had normal numbers of PGCs, whereas others had very few. Quantification of this phenotype showed a clear increase in variance in PGC number (Figure 2, A and B; P < 0.001 for miR-969; P < 0.05 for miR-9c). Increased variance also was rescued by restoring maternal expression of the corresponding miRNA in the mutant background (Figure 2, A and B; P < 0.001 for miR-969; P < 0.05 for miR-9c). The magnitude of the variance observed in the rescued mutant embryos was comparable with that of the heterozygous mutant controls (Figure 2, A and B) and with that of the Oregon R and w1118 control embryos.


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

Kugler JM, Chen YW, Weng R, Cohen SM - G3 (Bethesda) (2013)

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-969KI;;T-969@Fb/+, (b) Df(1)BSC352/miR-969KI, 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-9cKO/miR-9cKO;T-9c@Fb/+, (e) miR-9cKO/miR-9cKO;+/nosGal4, (f) miR-9cKO/miR-9cKO;T-9c@Fb/nosGal4, (g) miR-9cKO/+;T-9c@Fb/+, and (h) +/miR-9cKO;+/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.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3755917&req=5

fig2: 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-969KI;;T-969@Fb/+, (b) Df(1)BSC352/miR-969KI, 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-9cKO/miR-9cKO;T-9c@Fb/+, (e) miR-9cKO/miR-9cKO;+/nosGal4, (f) miR-9cKO/miR-9cKO;T-9c@Fb/nosGal4, (g) miR-9cKO/+;T-9c@Fb/+, and (h) +/miR-9cKO;+/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.
Mentions: In addition, we noted that the range of PGC numbers was broader in embryos from the miRNA mutant mothers than from the controls. Some had normal numbers of PGCs, whereas others had very few. Quantification of this phenotype showed a clear increase in variance in PGC number (Figure 2, A and B; P < 0.001 for miR-969; P < 0.05 for miR-9c). Increased variance also was rescued by restoring maternal expression of the corresponding miRNA in the mutant background (Figure 2, A and B; P < 0.001 for miR-969; P < 0.05 for miR-9c). The magnitude of the variance observed in the rescued mutant embryos was comparable with that of the heterozygous mutant controls (Figure 2, A and B) and with that of the Oregon R and w1118 control embryos.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Molecular and Cell Biology, Singapore 138673, Republic of Singapore.

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.

Show MeSH