Abstract:Hybrids between species are often characterized by novel gene-expression patterns. A recent study on allele-specific gene expression in hybrids between species of Drosophila revealed cases in which cis-and transregulatory elements within species had coevolved in such a way that changes in cis-regulatory elements are compensated by changes in trans-regulatory elements. We hypothesized that such coevolution should often lead to gene misexpression in the hybrid. To test this hypothesis, we estimated allele-specif… Show more
“…We have shown in Table 1 that the contribution of interactive terms to expression variation between populations is Ͼ30% and can be as large as 50%. In the analysis of interspecific F 1 hybrids, Landry et al (5) have shown that 13 of the 23 misexpressed genes exhibited cis-bytrans interaction. Furthermore, cis and trans factors can interact in opposition to each other.…”
Section: Discussionmentioning
confidence: 99%
“…(cis regulation refers to the control of expression by the gene itself whereas trans regulation refers to the influence of the genetic background.) Many studies have addressed this question at various levels of divergence (1)(2)(3)(4)(5)(6)(7)(8)(9). For example, one may measure the expressions of two alleles at the locus of interest in a common genetic background (usually F 1 s) (1,2,5).…”
Regulation of gene expression is usually separated into cis and trans components. The separation may become artificial if much of the variation in expression is under multigenic and epistatic (e.g., cis-bytrans) control. There is hence a need to quantify the relative contribution of cis, trans, and cis-by-trans effects on expression divergence at different levels of evolution. To do so across the whole genome, we analyzed the full set of chromosome-substitution lines between the two behavioral races of Drosophila melanogaster. Our observations: (i) Only Ϸ3% of the genes with an expression difference are purely cis regulated. In fact, relatively few genes are governed by simple genetics because nearly 80% of expression differences are controlled by at least two chromosomes. (ii) For 14% of the genes, cis regulation does play a role but usually in conjunction with trans regulation. This joint action of cis and trans effects, either additive or epistatic, is referred to as inclusive cis effect. (iii) The percentage of genes with inclusive cis effect increases to 32% among genes that are strongly differentiated between the two races. (iv) We observed a nonrandom distribution of trans-acting factors, with a substantial deficit on the second chromosome. Between Drosophila racial groups, trans regulation of expression difference is extensive, and cis regulation often evolves in conjunction with trans effects.K nowledge of the genetics of complex traits is fundamental to modern medicine, agriculture, and evolutionary biology. Among all complex traits, gene expression as phenotype may be most amenable to genetic analysis. The first question about expression regulation naturally is whether there is a cis component and how strong the cis component is. (cis regulation refers to the control of expression by the gene itself whereas trans regulation refers to the influence of the genetic background.) Many studies have addressed this question at various levels of divergence (1-9). For example, one may measure the expressions of two alleles at the locus of interest in a common genetic background (usually F 1 s) (1, 2, 5). Because the collection of trans-acting factors in the same cellular environment is assumed to affect the two alleles equally, asymmetric allelic expression implies differences due to cis-regulatory divergence. Similarly, expression quantitative trait loci (eQTL) mapping permits inference of cis regulation if the eQTL is mapped closely to the expressed gene itself (6-10).A second question is how strong cis regulation is relative to trans regulation. In the extreme case where most expression variation is controlled by cis-trans interactions (e.g., joint actions of cis elements and transcription factors), the question would not be very meaningful because cis and trans components are both indispensable. It is desirable to explicitly model expression regulation to include cis, trans, and cis-by-trans control. Many kinds of data allow such explicit modeling. The use of large numbers of recombinant strains for express...
“…We have shown in Table 1 that the contribution of interactive terms to expression variation between populations is Ͼ30% and can be as large as 50%. In the analysis of interspecific F 1 hybrids, Landry et al (5) have shown that 13 of the 23 misexpressed genes exhibited cis-bytrans interaction. Furthermore, cis and trans factors can interact in opposition to each other.…”
Section: Discussionmentioning
confidence: 99%
“…(cis regulation refers to the control of expression by the gene itself whereas trans regulation refers to the influence of the genetic background.) Many studies have addressed this question at various levels of divergence (1)(2)(3)(4)(5)(6)(7)(8)(9). For example, one may measure the expressions of two alleles at the locus of interest in a common genetic background (usually F 1 s) (1,2,5).…”
Regulation of gene expression is usually separated into cis and trans components. The separation may become artificial if much of the variation in expression is under multigenic and epistatic (e.g., cis-bytrans) control. There is hence a need to quantify the relative contribution of cis, trans, and cis-by-trans effects on expression divergence at different levels of evolution. To do so across the whole genome, we analyzed the full set of chromosome-substitution lines between the two behavioral races of Drosophila melanogaster. Our observations: (i) Only Ϸ3% of the genes with an expression difference are purely cis regulated. In fact, relatively few genes are governed by simple genetics because nearly 80% of expression differences are controlled by at least two chromosomes. (ii) For 14% of the genes, cis regulation does play a role but usually in conjunction with trans regulation. This joint action of cis and trans effects, either additive or epistatic, is referred to as inclusive cis effect. (iii) The percentage of genes with inclusive cis effect increases to 32% among genes that are strongly differentiated between the two races. (iv) We observed a nonrandom distribution of trans-acting factors, with a substantial deficit on the second chromosome. Between Drosophila racial groups, trans regulation of expression difference is extensive, and cis regulation often evolves in conjunction with trans effects.K nowledge of the genetics of complex traits is fundamental to modern medicine, agriculture, and evolutionary biology. Among all complex traits, gene expression as phenotype may be most amenable to genetic analysis. The first question about expression regulation naturally is whether there is a cis component and how strong the cis component is. (cis regulation refers to the control of expression by the gene itself whereas trans regulation refers to the influence of the genetic background.) Many studies have addressed this question at various levels of divergence (1-9). For example, one may measure the expressions of two alleles at the locus of interest in a common genetic background (usually F 1 s) (1, 2, 5). Because the collection of trans-acting factors in the same cellular environment is assumed to affect the two alleles equally, asymmetric allelic expression implies differences due to cis-regulatory divergence. Similarly, expression quantitative trait loci (eQTL) mapping permits inference of cis regulation if the eQTL is mapped closely to the expressed gene itself (6-10).A second question is how strong cis regulation is relative to trans regulation. In the extreme case where most expression variation is controlled by cis-trans interactions (e.g., joint actions of cis elements and transcription factors), the question would not be very meaningful because cis and trans components are both indispensable. It is desirable to explicitly model expression regulation to include cis, trans, and cis-by-trans control. Many kinds of data allow such explicit modeling. The use of large numbers of recombinant strains for express...
“…Here, because allelic expression was analyzed in hybrids, only cis-regulatory differences could be detected. In order to detect trans-regulatory effects, it would have been necessary to study allelic expression in not only hybrids but also parental populations at the same life stage, which was not possible here (Wittkopp et al, 2004;Landry et al, 2005;Fraser et al, 2011). We therefore preferred to increase coverage for the hybrid crosses in order to at least more rigorously confirm the occurrence of cis regulation, as directly reflected by significant allelic imbalance in hybrids.…”
Section: Cis-acting Regulatory Effectsmentioning
confidence: 99%
“…For example, dominance in gene expression inheritance has been significantly associated with trans regulatory elements (Lemos et al, 2008). Finally, gene expression regulation can be affected by the interaction of both regulatory systems, either through trans by trans or through cis by trans interactions (Landry et al, 2005).…”
Section: Introductionmentioning
confidence: 99%
“…Allelic imbalance is caused by the direct influence of cis-regulatory elements. On the other hand, we may conclude to the presence of trans-regulatory effects when the following two conditions are met: (1) no allelic imbalance is observed in heterozygous individuals, as trans-regulatory elements affect both alleles in the same manner, and (2) when homozygous individuals possessing the same allele and originating from different populations show differences in allelic expression levels (Wittkopp et al, 2004;Landry et al, 2005).…”
Hybridization can lead to phenotypic differences arising from changes in gene expression patterns or new allele combinations. Variation in gene expression is thought to be controlled by differences in transcription regulation of parental alleles, either through cis-or trans-regulatory elements. A previous study among brook charr hybrids from different populations (Rupert, Laval, and domestic) showing distinct length at age during early life stages also revealed different patterns in transcription regulation inheritance of transcript abundance. In the present study, transcript abundance using RNA-sequencing and quantitative real-time PCR, single-nucleotide polymorphism (SNP) genotypes and allelic imbalance were assessed in order to understand the molecular mechanisms underlying the observed transcriptomic and differences in length at age among domestic  Rupert hybrids and Laval  domestic hybrids. We found 198 differentially expressed genes between the two hybrid crosses, and allelic imbalance could be analyzed for 69 of them. Among these 69 genes, 36 genes exhibited cis-acting regulatory effects in both of the two crosses, thus confirming the prevalent role of cis-acting regulatory elements in the regulation of differentially expressed genes among intraspecific hybrids. In addition, we detected a significant association between SNP genotypes of three genes and length at age. Our study is thus one of the few that have highlighted some of the molecular mechanisms potentially involved in the differential phenotypic expression in intraspecific hybrids for nonmodel species.
Sex chromosomes, particularly the X chromosome, play a unique role in evolution due to several distinct features. In
Drosophila
, the X chromosome has been proposed to constitute an undesirable environment for genes expressed at higher levels in males than in females (i.e. male‐biased genes) and, as a result, is partially demasculinized. However, male‐biased genes remaining on the X chromosome do not seem to be at a disadvantage relative to their autosomal counterparts. Population genetic models predict that under certain conditions X‐linked genes will experience more bouts of positive selection than autosomal genes, leading to faster‐X evolution, particularly for male‐biased genes. As theory posits,
Drosophila
X‐linked male‐biased genes show evidence of adaptive evolution at both protein and expression levels. This faster‐X evolution has broad implications. In speciation, it may contribute to explain why the X chromosome is a hotspot for the genetic factors underlying hybrid male sterility (i.e. the large X‐effect).
Key Concepts:
Underrepresentation of X‐linked male‐biased genes due to unfavorable features of the X chromosome.
Faster‐X evolution of male‐biased genes at both the protein and expression levels.
Consequences of faster‐X evolution include the disproportionally large effect of the X chromosome in hybrid male sterility.
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