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Transvection-based gene regulation in Drosophila is a complex and plastic trait.

Bing X, Rzezniczak TZ, Bateman JR, Merritt TJ - G3 (Bethesda) (2014)

Bottom Line: We further show that the magnitude of transvection at the Men locus is modified by both genetic background and environment (temperature), demonstrating that transvection is a plastic phenotype.Our results suggest that transvection effects in D. melanogaster are shaped by a dynamic interplay between environment and genetic background.Interestingly, we find that cis-based regulation of the Men gene is more robust to genetic background and environment than trans-based.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry and Biochemistry, Laurentian University, Sudbury, ON, P3E 2C6, Canada.

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Putative transcription factor binding sites (TFBSs) that may participate in gene regulation and transvection at the Men locus. (A) Colored circles indicate putative TFBSs for the five genes we have analyzed in our study: Abd-B, Iroquois, C/EBP-like bZIP TF, GAGA element, and zeste. For each MenExi− allele, we indicate the excised region with bracket dotted lines. Faded circles represent TFBSs unique to an excision allele (in MenEx58− and MenEx60−). (B) Detail of the excision site of MenEx58− and MenEx60−, two alleles that differ in deletion size by ~100 bp and significantly differ in their ability to drive transvection. Each allele has a unique insertion at the excision site: MenEx58− has an additional Iroquois site; MenEx60− has an additional Abd-B site. TFBSs circled in red correspond to transcription factor genes analyzed with quantitative reverse-transcription polymerase chain reaction.
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fig5: Putative transcription factor binding sites (TFBSs) that may participate in gene regulation and transvection at the Men locus. (A) Colored circles indicate putative TFBSs for the five genes we have analyzed in our study: Abd-B, Iroquois, C/EBP-like bZIP TF, GAGA element, and zeste. For each MenExi− allele, we indicate the excised region with bracket dotted lines. Faded circles represent TFBSs unique to an excision allele (in MenEx58− and MenEx60−). (B) Detail of the excision site of MenEx58− and MenEx60−, two alleles that differ in deletion size by ~100 bp and significantly differ in their ability to drive transvection. Each allele has a unique insertion at the excision site: MenEx58− has an additional Iroquois site; MenEx60− has an additional Abd-B site. TFBSs circled in red correspond to transcription factor genes analyzed with quantitative reverse-transcription polymerase chain reaction.

Mentions: The differences in transvection we observed across excision alleles, genetic backgrounds, and holding temperatures could be functions of the presence or absence of TFBS (i.e., local factors) and/or differences in the activity of TF (i.e., distant factors) between alleles and backgrounds. A number of predicted TFBS near the Men transcription start site are deleted, retained, or inserted in different MenExi− alleles, and the presence or absence of these elements may drive or modify differences in trans-activity observed between alleles (Figure 5A; Lum and Merritt 2011). To investigate this possibility, we focused on two excision alleles, MenEx60− and MenEx58−: alleles that differ significantly in their ability to drive transvection but only by approximately 100 bp in excision size (Figure 1; Lum and Merritt 2011). MenEx60− is also of particular interest because it consistently drives greater than 100% wild-type MEN activity when heterozygous with a wild-type chromosome. Figure 5B diagrams the excision sites of these two alleles, indicating TFBS that have high matrix similarity (>0.90 core matrix similarity to optimal transcription factor binding matrix). Two putative TFBSs are found in MenEx58−, but not MenEx60−: C/EBP-like bZIP and Iroquois. C/EBP-like bZIP can be bound by the transcription factor Slowbordercells (Slbo), and Iroquois can be bound by Mirror (Bilioni et al. 2005; Murphy et al. 1995). Additionally, one putative TFBS is found in MenEx60−, but not MenEx58−: Abd-B, which can be bound by Abdominal-B protein (Abd-B; Ekker et al. 1994). The Iroquois and Abd-B binding sites are not found in the wild-type genomic sequence and result from the P-element insertion/excision events. Similar P-element remnant sequences have been shown to modify transvection at other loci (yellow; Geyer et al. 1990; Gpdh; Gibson et al. 1999). We suspected that the differential transvection ability of these two alleles could be a function of these distinct sites through differential responses of the two alleles to levels of the respective binding proteins. Finally, two predicted TFBS that are found in the wild-type sequence are deleted in both MenEx60− and MenEx58−: GAGA element and zeste. GAGA and zeste sites can be bound by Trithorax-like (Trl; van Steensel et al. 2003) and zeste (z; Benson and Pirrotta 1988), respectively. Given the differences between MenEx60− and MenEx58− in C/EBP like bZIP, Iroquois, and Abd-B, but not GAGA and zeste binding sites, we predicted that, if these binding sites are functional, the differences in transvection observed between the two alleles across the genetic backgrounds and temperatures could correlate with differences in slbo, mirr, or Abd-B expression, but not Trl or z expression.


Transvection-based gene regulation in Drosophila is a complex and plastic trait.

Bing X, Rzezniczak TZ, Bateman JR, Merritt TJ - G3 (Bethesda) (2014)

Putative transcription factor binding sites (TFBSs) that may participate in gene regulation and transvection at the Men locus. (A) Colored circles indicate putative TFBSs for the five genes we have analyzed in our study: Abd-B, Iroquois, C/EBP-like bZIP TF, GAGA element, and zeste. For each MenExi− allele, we indicate the excised region with bracket dotted lines. Faded circles represent TFBSs unique to an excision allele (in MenEx58− and MenEx60−). (B) Detail of the excision site of MenEx58− and MenEx60−, two alleles that differ in deletion size by ~100 bp and significantly differ in their ability to drive transvection. Each allele has a unique insertion at the excision site: MenEx58− has an additional Iroquois site; MenEx60− has an additional Abd-B site. TFBSs circled in red correspond to transcription factor genes analyzed with quantitative reverse-transcription polymerase chain reaction.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4232543&req=5

fig5: Putative transcription factor binding sites (TFBSs) that may participate in gene regulation and transvection at the Men locus. (A) Colored circles indicate putative TFBSs for the five genes we have analyzed in our study: Abd-B, Iroquois, C/EBP-like bZIP TF, GAGA element, and zeste. For each MenExi− allele, we indicate the excised region with bracket dotted lines. Faded circles represent TFBSs unique to an excision allele (in MenEx58− and MenEx60−). (B) Detail of the excision site of MenEx58− and MenEx60−, two alleles that differ in deletion size by ~100 bp and significantly differ in their ability to drive transvection. Each allele has a unique insertion at the excision site: MenEx58− has an additional Iroquois site; MenEx60− has an additional Abd-B site. TFBSs circled in red correspond to transcription factor genes analyzed with quantitative reverse-transcription polymerase chain reaction.
Mentions: The differences in transvection we observed across excision alleles, genetic backgrounds, and holding temperatures could be functions of the presence or absence of TFBS (i.e., local factors) and/or differences in the activity of TF (i.e., distant factors) between alleles and backgrounds. A number of predicted TFBS near the Men transcription start site are deleted, retained, or inserted in different MenExi− alleles, and the presence or absence of these elements may drive or modify differences in trans-activity observed between alleles (Figure 5A; Lum and Merritt 2011). To investigate this possibility, we focused on two excision alleles, MenEx60− and MenEx58−: alleles that differ significantly in their ability to drive transvection but only by approximately 100 bp in excision size (Figure 1; Lum and Merritt 2011). MenEx60− is also of particular interest because it consistently drives greater than 100% wild-type MEN activity when heterozygous with a wild-type chromosome. Figure 5B diagrams the excision sites of these two alleles, indicating TFBS that have high matrix similarity (>0.90 core matrix similarity to optimal transcription factor binding matrix). Two putative TFBSs are found in MenEx58−, but not MenEx60−: C/EBP-like bZIP and Iroquois. C/EBP-like bZIP can be bound by the transcription factor Slowbordercells (Slbo), and Iroquois can be bound by Mirror (Bilioni et al. 2005; Murphy et al. 1995). Additionally, one putative TFBS is found in MenEx60−, but not MenEx58−: Abd-B, which can be bound by Abdominal-B protein (Abd-B; Ekker et al. 1994). The Iroquois and Abd-B binding sites are not found in the wild-type genomic sequence and result from the P-element insertion/excision events. Similar P-element remnant sequences have been shown to modify transvection at other loci (yellow; Geyer et al. 1990; Gpdh; Gibson et al. 1999). We suspected that the differential transvection ability of these two alleles could be a function of these distinct sites through differential responses of the two alleles to levels of the respective binding proteins. Finally, two predicted TFBS that are found in the wild-type sequence are deleted in both MenEx60− and MenEx58−: GAGA element and zeste. GAGA and zeste sites can be bound by Trithorax-like (Trl; van Steensel et al. 2003) and zeste (z; Benson and Pirrotta 1988), respectively. Given the differences between MenEx60− and MenEx58− in C/EBP like bZIP, Iroquois, and Abd-B, but not GAGA and zeste binding sites, we predicted that, if these binding sites are functional, the differences in transvection observed between the two alleles across the genetic backgrounds and temperatures could correlate with differences in slbo, mirr, or Abd-B expression, but not Trl or z expression.

Bottom Line: We further show that the magnitude of transvection at the Men locus is modified by both genetic background and environment (temperature), demonstrating that transvection is a plastic phenotype.Our results suggest that transvection effects in D. melanogaster are shaped by a dynamic interplay between environment and genetic background.Interestingly, we find that cis-based regulation of the Men gene is more robust to genetic background and environment than trans-based.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry and Biochemistry, Laurentian University, Sudbury, ON, P3E 2C6, Canada.

Show MeSH
Related in: MedlinePlus