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Adaptive evolution of genes involved in the regulation of germline stem cells in Drosophila melanogaster and D. simulans.

Flores HA, DuMont VL, Fatoo A, Hubbard D, Hijji M, Barbash DA, Aquadro CF - G3 (Bethesda) (2015)

Bottom Line: Population genetic and comparative analyses in diverse taxa have shown that numerous genes involved in reproduction are adaptively evolving.Two genes involved in germline stem cell regulation, bag of marbles (bam) and benign gonial cell neoplasm (bgcn), have been shown previously to experience recurrent, adaptive evolution in both Drosophila melanogaster and D. simulans.Here we report a population genetic survey on eight additional genes involved in germline stem cell regulation in D. melanogaster and D. simulans that reveals all eight of these genes reject a neutral model of evolution in at least one test and one species after correction for multiple testing using a false-discovery rate of 0.05.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853.

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Schematic of the Drosophila ovarian germline stem cell (GSC) niche with genes analyzed. Adapted from Wong et al. (2005). The GSC (light blue cell) is present in a niche environment (green cells are somatic cap and terminal filament cells, yellow cells are escort stem cells) required to maintain its stem cell state. Bam is repressed in the GSC. Only when the GSC moves away from the niche is Bam expressed and this cell starts to differentiate (tan cell). Yb is involved in the maintenance of GSCs and regulating their division. Piwi acts cell nonautonomously to help in the repression of Bam in the GSC. Zpg is an adherens junction protein that functions in cell signaling. Nos and Pum act as translational repressors of genes that will promote differentiation. Mei-p26 acts in concert with the miRNA machinery (miRISC in the figure) to also repress transcripts (indicated by red squiggly lines), some of which are shared with Nos and Pum. Bgcn is required for Bam to cause GSCs to differentiate. Bam and Bgcn antagonize the Nos/Pum complex. Stwl represses Bam-independent differentiation pathways and thus maintains GSC self-renewal. The cystoblast (tan cell) will undergo four mitotic divisions. CycA participates in the regulation of these mitotic divisions but is not shown in this diagram.
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fig1: Schematic of the Drosophila ovarian germline stem cell (GSC) niche with genes analyzed. Adapted from Wong et al. (2005). The GSC (light blue cell) is present in a niche environment (green cells are somatic cap and terminal filament cells, yellow cells are escort stem cells) required to maintain its stem cell state. Bam is repressed in the GSC. Only when the GSC moves away from the niche is Bam expressed and this cell starts to differentiate (tan cell). Yb is involved in the maintenance of GSCs and regulating their division. Piwi acts cell nonautonomously to help in the repression of Bam in the GSC. Zpg is an adherens junction protein that functions in cell signaling. Nos and Pum act as translational repressors of genes that will promote differentiation. Mei-p26 acts in concert with the miRNA machinery (miRISC in the figure) to also repress transcripts (indicated by red squiggly lines), some of which are shared with Nos and Pum. Bgcn is required for Bam to cause GSCs to differentiate. Bam and Bgcn antagonize the Nos/Pum complex. Stwl represses Bam-independent differentiation pathways and thus maintains GSC self-renewal. The cystoblast (tan cell) will undergo four mitotic divisions. CycA participates in the regulation of these mitotic divisions but is not shown in this diagram.

Mentions: There have been several genome-wide, next-generation sequencing surveys of variation in D. melanogaster and D. simulans that have reported departures from an equilibrium neutral model in directions consistent with natural selection for GSC-related gene ontology categories or at/near several GSC genes (Begun et al. 2007; Langley et al. 2012; Pool et al. 2012). It remains informative to examine specific genes, particularly using parallel assays on population data from both D. melanogaster and D. simulans. Here, we report high-quality Sanger resequencing from population samples of both species for eight genes involved in GSC regulation (cyclin A, mei-P26, nanos, P-element induced wimpy testis (aka piwi), pumilio, stonewall, fs(1)Yb, and zero population growth), test for evidence of selection using polymorphism-based methods and reanalyze longer-term sequence evolution at these genes using phylogenetic analysis by maximum likelihood (PAML). These eight genes include those whose products genetically and/or physically interact with bam and/or bgcn and are likely to have shared functions, and those that appear to have non-bam/bgcn-related roles in GSC regulation. Figure 1 illustrates the roles of these loci within the female germline, wherein the functions and interactions of these genes are more thoroughly understood. We note that several of these genes function somewhat differently in the male germline (Fuller and Spradling 2007; Gilboa and Lehmann 2004; Gonczy et al. 1997; Insco et al. 2009; Kawase et al. 2004; Song et al. 2004).


Adaptive evolution of genes involved in the regulation of germline stem cells in Drosophila melanogaster and D. simulans.

Flores HA, DuMont VL, Fatoo A, Hubbard D, Hijji M, Barbash DA, Aquadro CF - G3 (Bethesda) (2015)

Schematic of the Drosophila ovarian germline stem cell (GSC) niche with genes analyzed. Adapted from Wong et al. (2005). The GSC (light blue cell) is present in a niche environment (green cells are somatic cap and terminal filament cells, yellow cells are escort stem cells) required to maintain its stem cell state. Bam is repressed in the GSC. Only when the GSC moves away from the niche is Bam expressed and this cell starts to differentiate (tan cell). Yb is involved in the maintenance of GSCs and regulating their division. Piwi acts cell nonautonomously to help in the repression of Bam in the GSC. Zpg is an adherens junction protein that functions in cell signaling. Nos and Pum act as translational repressors of genes that will promote differentiation. Mei-p26 acts in concert with the miRNA machinery (miRISC in the figure) to also repress transcripts (indicated by red squiggly lines), some of which are shared with Nos and Pum. Bgcn is required for Bam to cause GSCs to differentiate. Bam and Bgcn antagonize the Nos/Pum complex. Stwl represses Bam-independent differentiation pathways and thus maintains GSC self-renewal. The cystoblast (tan cell) will undergo four mitotic divisions. CycA participates in the regulation of these mitotic divisions but is not shown in this diagram.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4390574&req=5

fig1: Schematic of the Drosophila ovarian germline stem cell (GSC) niche with genes analyzed. Adapted from Wong et al. (2005). The GSC (light blue cell) is present in a niche environment (green cells are somatic cap and terminal filament cells, yellow cells are escort stem cells) required to maintain its stem cell state. Bam is repressed in the GSC. Only when the GSC moves away from the niche is Bam expressed and this cell starts to differentiate (tan cell). Yb is involved in the maintenance of GSCs and regulating their division. Piwi acts cell nonautonomously to help in the repression of Bam in the GSC. Zpg is an adherens junction protein that functions in cell signaling. Nos and Pum act as translational repressors of genes that will promote differentiation. Mei-p26 acts in concert with the miRNA machinery (miRISC in the figure) to also repress transcripts (indicated by red squiggly lines), some of which are shared with Nos and Pum. Bgcn is required for Bam to cause GSCs to differentiate. Bam and Bgcn antagonize the Nos/Pum complex. Stwl represses Bam-independent differentiation pathways and thus maintains GSC self-renewal. The cystoblast (tan cell) will undergo four mitotic divisions. CycA participates in the regulation of these mitotic divisions but is not shown in this diagram.
Mentions: There have been several genome-wide, next-generation sequencing surveys of variation in D. melanogaster and D. simulans that have reported departures from an equilibrium neutral model in directions consistent with natural selection for GSC-related gene ontology categories or at/near several GSC genes (Begun et al. 2007; Langley et al. 2012; Pool et al. 2012). It remains informative to examine specific genes, particularly using parallel assays on population data from both D. melanogaster and D. simulans. Here, we report high-quality Sanger resequencing from population samples of both species for eight genes involved in GSC regulation (cyclin A, mei-P26, nanos, P-element induced wimpy testis (aka piwi), pumilio, stonewall, fs(1)Yb, and zero population growth), test for evidence of selection using polymorphism-based methods and reanalyze longer-term sequence evolution at these genes using phylogenetic analysis by maximum likelihood (PAML). These eight genes include those whose products genetically and/or physically interact with bam and/or bgcn and are likely to have shared functions, and those that appear to have non-bam/bgcn-related roles in GSC regulation. Figure 1 illustrates the roles of these loci within the female germline, wherein the functions and interactions of these genes are more thoroughly understood. We note that several of these genes function somewhat differently in the male germline (Fuller and Spradling 2007; Gilboa and Lehmann 2004; Gonczy et al. 1997; Insco et al. 2009; Kawase et al. 2004; Song et al. 2004).

Bottom Line: Population genetic and comparative analyses in diverse taxa have shown that numerous genes involved in reproduction are adaptively evolving.Two genes involved in germline stem cell regulation, bag of marbles (bam) and benign gonial cell neoplasm (bgcn), have been shown previously to experience recurrent, adaptive evolution in both Drosophila melanogaster and D. simulans.Here we report a population genetic survey on eight additional genes involved in germline stem cell regulation in D. melanogaster and D. simulans that reveals all eight of these genes reject a neutral model of evolution in at least one test and one species after correction for multiple testing using a false-discovery rate of 0.05.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853.

Show MeSH
Related in: MedlinePlus