Limits...
Biased Allele Expression and Aggression in Hybrid Honeybees may be Influenced by Inappropriate Nuclear-Cytoplasmic Signaling.

Gibson JD, Arechavaleta-Velasco ME, Tsuruda JM, Hunt GJ - Front Genet (2015)

Bottom Line: This asymmetrically biased set is enriched for genes in loci associated with aggressive behavior and also for mitochondrial-localizing proteins.It contains many genes that play important roles in metabolic regulation.Moreover we find genes relating to the piwi-interacting RNA (piRNA) pathway, which is involved in chromatin modifications and epigenetic regulation and may help explain the mechanism underlying this asymmetric allele use.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Purdue University, West Lafayette IN, USA.

ABSTRACT
Hybrid effects are often exhibited asymmetrically between reciprocal families. One way this could happen is if silencing of one parent's allele occurs in one lineage but not the other, which could affect the phenotypes of the hybrids asymmetrically by silencing that allele in only one of the hybrid families. We have previously tested for allele-specific expression biases in hybrids of European and Africanized honeybees and we found that there was an asymmetric overabundance of genes showing a maternal bias in the family with a European mother. Here, we further analyze allelic bias in these hybrids to ascertain whether they may underlie previously described asymmetries in metabolism and aggression in similar hybrid families and we speculate on what mechanisms may produce this biased allele usage. We find that there are over 500 genes that have some form of biased allele usage and over 200 of these are biased toward the maternal allele but only in the family with European maternity, mirroring the pattern observed for aggression and metabolic rate. This asymmetrically biased set is enriched for genes in loci associated with aggressive behavior and also for mitochondrial-localizing proteins. It contains many genes that play important roles in metabolic regulation. Moreover we find genes relating to the piwi-interacting RNA (piRNA) pathway, which is involved in chromatin modifications and epigenetic regulation and may help explain the mechanism underlying this asymmetric allele use. Based on these findings and previous work investigating aggression and metabolism in bees, we propose a novel hypothesis; that the asymmetric pattern of biased allele usage in these hybrids is a result of inappropriate use of piRNA-mediated nuclear-cytoplasmic signaling that is normally used to modulate aggression in honeybees. This is the first report of widespread asymmetric effects on allelic expression in hybrids and may represent a novel mechanism for gene regulation.

No MeSH data available.


Related in: MedlinePlus

Heat map of maternally biased gene clusters. (A) Gene cluster on chromosome 3, overlapping a QTL associated with stinging behavior. (B) Gene cluster on chromosome 12, overlapping a QTL associated with alarm pheromone production (isopentyl acetate). Position along the chromosome (in Mbp), relative allele usage of each reciprocal family within each sample, and OGS 3.2 gene ID is given for every tested gene within these clusters. Relative allele usage calculated as maternal read count/total read count. ∗Statistically significant allelic bias. NT, not tested. N/A in gene ID column are transcripts that had no clear match to a protein coding gene.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4664729&req=5

Figure 3: Heat map of maternally biased gene clusters. (A) Gene cluster on chromosome 3, overlapping a QTL associated with stinging behavior. (B) Gene cluster on chromosome 12, overlapping a QTL associated with alarm pheromone production (isopentyl acetate). Position along the chromosome (in Mbp), relative allele usage of each reciprocal family within each sample, and OGS 3.2 gene ID is given for every tested gene within these clusters. Relative allele usage calculated as maternal read count/total read count. ∗Statistically significant allelic bias. NT, not tested. N/A in gene ID column are transcripts that had no clear match to a protein coding gene.

Mentions: We identified two regions containing clusters of genes that all appear to be biased, both of which overlap with defense-related QTL. One on chromosome 3 lies within the Sting-2 QTL, a region associated with increased colony-level stinging behavior (Hunt et al., 1998, 2007). There are 12 genes within a region of ∼410 kb that show a significant maternal bias of greater than 90% in the European maternity family (Figure 3A). There is only one additional gene within this region that could be tested and this gene also shows >90% maternal bias in this family. The second cluster lies on chromosome 12 within the bounds of a QTL associated with production of the active component of alarm pheromone, isopentyl acetate (Hunt et al., 1999). This region is ∼600 kb in length and there are 29 genes that could be tested within this region. Similar to the cluster within the Sting-2 QTL, 27 of these genes show a significant maternal bias (>90% maternal in 23 of these genes) in the European maternity family and the remaining two genes show the same pattern of extreme maternal bias (Figure 3B).


Biased Allele Expression and Aggression in Hybrid Honeybees may be Influenced by Inappropriate Nuclear-Cytoplasmic Signaling.

Gibson JD, Arechavaleta-Velasco ME, Tsuruda JM, Hunt GJ - Front Genet (2015)

Heat map of maternally biased gene clusters. (A) Gene cluster on chromosome 3, overlapping a QTL associated with stinging behavior. (B) Gene cluster on chromosome 12, overlapping a QTL associated with alarm pheromone production (isopentyl acetate). Position along the chromosome (in Mbp), relative allele usage of each reciprocal family within each sample, and OGS 3.2 gene ID is given for every tested gene within these clusters. Relative allele usage calculated as maternal read count/total read count. ∗Statistically significant allelic bias. NT, not tested. N/A in gene ID column are transcripts that had no clear match to a protein coding gene.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4664729&req=5

Figure 3: Heat map of maternally biased gene clusters. (A) Gene cluster on chromosome 3, overlapping a QTL associated with stinging behavior. (B) Gene cluster on chromosome 12, overlapping a QTL associated with alarm pheromone production (isopentyl acetate). Position along the chromosome (in Mbp), relative allele usage of each reciprocal family within each sample, and OGS 3.2 gene ID is given for every tested gene within these clusters. Relative allele usage calculated as maternal read count/total read count. ∗Statistically significant allelic bias. NT, not tested. N/A in gene ID column are transcripts that had no clear match to a protein coding gene.
Mentions: We identified two regions containing clusters of genes that all appear to be biased, both of which overlap with defense-related QTL. One on chromosome 3 lies within the Sting-2 QTL, a region associated with increased colony-level stinging behavior (Hunt et al., 1998, 2007). There are 12 genes within a region of ∼410 kb that show a significant maternal bias of greater than 90% in the European maternity family (Figure 3A). There is only one additional gene within this region that could be tested and this gene also shows >90% maternal bias in this family. The second cluster lies on chromosome 12 within the bounds of a QTL associated with production of the active component of alarm pheromone, isopentyl acetate (Hunt et al., 1999). This region is ∼600 kb in length and there are 29 genes that could be tested within this region. Similar to the cluster within the Sting-2 QTL, 27 of these genes show a significant maternal bias (>90% maternal in 23 of these genes) in the European maternity family and the remaining two genes show the same pattern of extreme maternal bias (Figure 3B).

Bottom Line: This asymmetrically biased set is enriched for genes in loci associated with aggressive behavior and also for mitochondrial-localizing proteins.It contains many genes that play important roles in metabolic regulation.Moreover we find genes relating to the piwi-interacting RNA (piRNA) pathway, which is involved in chromatin modifications and epigenetic regulation and may help explain the mechanism underlying this asymmetric allele use.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Purdue University, West Lafayette IN, USA.

ABSTRACT
Hybrid effects are often exhibited asymmetrically between reciprocal families. One way this could happen is if silencing of one parent's allele occurs in one lineage but not the other, which could affect the phenotypes of the hybrids asymmetrically by silencing that allele in only one of the hybrid families. We have previously tested for allele-specific expression biases in hybrids of European and Africanized honeybees and we found that there was an asymmetric overabundance of genes showing a maternal bias in the family with a European mother. Here, we further analyze allelic bias in these hybrids to ascertain whether they may underlie previously described asymmetries in metabolism and aggression in similar hybrid families and we speculate on what mechanisms may produce this biased allele usage. We find that there are over 500 genes that have some form of biased allele usage and over 200 of these are biased toward the maternal allele but only in the family with European maternity, mirroring the pattern observed for aggression and metabolic rate. This asymmetrically biased set is enriched for genes in loci associated with aggressive behavior and also for mitochondrial-localizing proteins. It contains many genes that play important roles in metabolic regulation. Moreover we find genes relating to the piwi-interacting RNA (piRNA) pathway, which is involved in chromatin modifications and epigenetic regulation and may help explain the mechanism underlying this asymmetric allele use. Based on these findings and previous work investigating aggression and metabolism in bees, we propose a novel hypothesis; that the asymmetric pattern of biased allele usage in these hybrids is a result of inappropriate use of piRNA-mediated nuclear-cytoplasmic signaling that is normally used to modulate aggression in honeybees. This is the first report of widespread asymmetric effects on allelic expression in hybrids and may represent a novel mechanism for gene regulation.

No MeSH data available.


Related in: MedlinePlus