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The evolutionary origination and diversification of a dimorphic gene regulatory network through parallel innovations in cis and trans.

Camino EM, Butts JC, Ordway A, Vellky JE, Rebeiz M, Williams TM - PLoS Genet. (2015)

Bottom Line: Morphological traits result from gene regulatory networks (GRNs) that form a web of transcription factors, which regulate multiple cis-regulatory element (CRE) sequences to control the coordinated expression of differentiation genes.By elucidating how yellow and tan are connected to the web of abdominal trans-regulators, we discovered that the yellow and tan abdominal CREs are composed of distinct regulatory inputs that exhibit contrasting responses to the same Hox proteins and Hox cofactors.These results provide an example in which CRE origination underlies a recently evolved novel trait, and highlights how coordinated expression patterns can evolve in parallel through the generation of unique regulatory linkages.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Dayton, Dayton, Ohio, United States of America.

ABSTRACT
The origination and diversification of morphological characteristics represents a key problem in understanding the evolution of development. Morphological traits result from gene regulatory networks (GRNs) that form a web of transcription factors, which regulate multiple cis-regulatory element (CRE) sequences to control the coordinated expression of differentiation genes. The formation and modification of GRNs must ultimately be understood at the level of individual regulatory linkages (i.e., transcription factor binding sites within CREs) that constitute the network. Here, we investigate how elements within a network originated and diversified to generate a broad range of abdominal pigmentation phenotypes among Sophophora fruit flies. Our data indicates that the coordinated expression of two melanin synthesis enzymes, Yellow and Tan, recently evolved through novel CRE activities that respond to the spatial patterning inputs of Hox proteins and the sex-specific input of Bric-à-brac transcription factors. Once established, it seems that these newly evolved activities were repeatedly modified by evolutionary changes in the network's trans-regulators to generate large-scale changes in pigment pattern. By elucidating how yellow and tan are connected to the web of abdominal trans-regulators, we discovered that the yellow and tan abdominal CREs are composed of distinct regulatory inputs that exhibit contrasting responses to the same Hox proteins and Hox cofactors. These results provide an example in which CRE origination underlies a recently evolved novel trait, and highlights how coordinated expression patterns can evolve in parallel through the generation of unique regulatory linkages.

No MeSH data available.


Related in: MedlinePlus

Gene network models for unpigmented and pigment abdominal segments.Wiring diagram of pigmentation gene networks experienced by the (A) non-melanic male A2-A4 segments and (B) the melanic A5 and A6 segments. (A) Abd-B expression is lacking in the anterior A2-A4 segments and as a result yellow and tan lack the direct and indirect activating input from this transcription factor. In these segments, Abd-A forms direct repressive inputs with tan which are supported (directly or indirectly) by the repressive effects of exd and hth. (B) Abd-B is expressed in the posterior A5 and A6 segments, where it acts as a direct activator of yellow and an indirect activator of tan. In these segments, Abd-A acts as an indirect activator of tan expression as well. In these schematics, inactive genes are indicated in gray coloring, solid connections between genes indicate validated direct interactions between a transcription factor and a pigmentation gene CRE, and dashed connections indicate indirect interactions or those not yet shown to be direct. Connections terminating with an arrowhead indicate connections in which the transcription factor functions as an activator, and connections terminating in a nail head shape indicate a repressive relationship.
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pgen.1005136.g007: Gene network models for unpigmented and pigment abdominal segments.Wiring diagram of pigmentation gene networks experienced by the (A) non-melanic male A2-A4 segments and (B) the melanic A5 and A6 segments. (A) Abd-B expression is lacking in the anterior A2-A4 segments and as a result yellow and tan lack the direct and indirect activating input from this transcription factor. In these segments, Abd-A forms direct repressive inputs with tan which are supported (directly or indirectly) by the repressive effects of exd and hth. (B) Abd-B is expressed in the posterior A5 and A6 segments, where it acts as a direct activator of yellow and an indirect activator of tan. In these segments, Abd-A acts as an indirect activator of tan expression as well. In these schematics, inactive genes are indicated in gray coloring, solid connections between genes indicate validated direct interactions between a transcription factor and a pigmentation gene CRE, and dashed connections indicate indirect interactions or those not yet shown to be direct. Connections terminating with an arrowhead indicate connections in which the transcription factor functions as an activator, and connections terminating in a nail head shape indicate a repressive relationship.

Mentions: Here, we have traced the evolutionary history of two CREs required for a novel trait, and show that they have recently evolved similar expression patterns through remarkably different architectures in a common trans-regulatory landscape. Our data indicates that the tergite-wide activities of the yBE and t_MSE did not exist in the monomorphic ancestor for Sophophora, but evolved in the lineage leading to the common ancestor of the melanogaster species group. Our results support a scenario where the subsequent expansion and contraction of male pigmentation pattern was driven primarily by alteration of the trans-regulators, whereas repeated losses involved both cis- and trans-evolution with respect to these CREs. Though the t_MSE and yBE drive coordinated patterns of gene expression, we found striking differences in their upstream regulators and direct regulatory linkages (Fig 7). These results bear on our understanding of how new gene regulatory networks form, diversify, and how coordinated regulatory activities can arise through the independent evolution of unique regulatory codes.


The evolutionary origination and diversification of a dimorphic gene regulatory network through parallel innovations in cis and trans.

Camino EM, Butts JC, Ordway A, Vellky JE, Rebeiz M, Williams TM - PLoS Genet. (2015)

Gene network models for unpigmented and pigment abdominal segments.Wiring diagram of pigmentation gene networks experienced by the (A) non-melanic male A2-A4 segments and (B) the melanic A5 and A6 segments. (A) Abd-B expression is lacking in the anterior A2-A4 segments and as a result yellow and tan lack the direct and indirect activating input from this transcription factor. In these segments, Abd-A forms direct repressive inputs with tan which are supported (directly or indirectly) by the repressive effects of exd and hth. (B) Abd-B is expressed in the posterior A5 and A6 segments, where it acts as a direct activator of yellow and an indirect activator of tan. In these segments, Abd-A acts as an indirect activator of tan expression as well. In these schematics, inactive genes are indicated in gray coloring, solid connections between genes indicate validated direct interactions between a transcription factor and a pigmentation gene CRE, and dashed connections indicate indirect interactions or those not yet shown to be direct. Connections terminating with an arrowhead indicate connections in which the transcription factor functions as an activator, and connections terminating in a nail head shape indicate a repressive relationship.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4383587&req=5

pgen.1005136.g007: Gene network models for unpigmented and pigment abdominal segments.Wiring diagram of pigmentation gene networks experienced by the (A) non-melanic male A2-A4 segments and (B) the melanic A5 and A6 segments. (A) Abd-B expression is lacking in the anterior A2-A4 segments and as a result yellow and tan lack the direct and indirect activating input from this transcription factor. In these segments, Abd-A forms direct repressive inputs with tan which are supported (directly or indirectly) by the repressive effects of exd and hth. (B) Abd-B is expressed in the posterior A5 and A6 segments, where it acts as a direct activator of yellow and an indirect activator of tan. In these segments, Abd-A acts as an indirect activator of tan expression as well. In these schematics, inactive genes are indicated in gray coloring, solid connections between genes indicate validated direct interactions between a transcription factor and a pigmentation gene CRE, and dashed connections indicate indirect interactions or those not yet shown to be direct. Connections terminating with an arrowhead indicate connections in which the transcription factor functions as an activator, and connections terminating in a nail head shape indicate a repressive relationship.
Mentions: Here, we have traced the evolutionary history of two CREs required for a novel trait, and show that they have recently evolved similar expression patterns through remarkably different architectures in a common trans-regulatory landscape. Our data indicates that the tergite-wide activities of the yBE and t_MSE did not exist in the monomorphic ancestor for Sophophora, but evolved in the lineage leading to the common ancestor of the melanogaster species group. Our results support a scenario where the subsequent expansion and contraction of male pigmentation pattern was driven primarily by alteration of the trans-regulators, whereas repeated losses involved both cis- and trans-evolution with respect to these CREs. Though the t_MSE and yBE drive coordinated patterns of gene expression, we found striking differences in their upstream regulators and direct regulatory linkages (Fig 7). These results bear on our understanding of how new gene regulatory networks form, diversify, and how coordinated regulatory activities can arise through the independent evolution of unique regulatory codes.

Bottom Line: Morphological traits result from gene regulatory networks (GRNs) that form a web of transcription factors, which regulate multiple cis-regulatory element (CRE) sequences to control the coordinated expression of differentiation genes.By elucidating how yellow and tan are connected to the web of abdominal trans-regulators, we discovered that the yellow and tan abdominal CREs are composed of distinct regulatory inputs that exhibit contrasting responses to the same Hox proteins and Hox cofactors.These results provide an example in which CRE origination underlies a recently evolved novel trait, and highlights how coordinated expression patterns can evolve in parallel through the generation of unique regulatory linkages.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Dayton, Dayton, Ohio, United States of America.

ABSTRACT
The origination and diversification of morphological characteristics represents a key problem in understanding the evolution of development. Morphological traits result from gene regulatory networks (GRNs) that form a web of transcription factors, which regulate multiple cis-regulatory element (CRE) sequences to control the coordinated expression of differentiation genes. The formation and modification of GRNs must ultimately be understood at the level of individual regulatory linkages (i.e., transcription factor binding sites within CREs) that constitute the network. Here, we investigate how elements within a network originated and diversified to generate a broad range of abdominal pigmentation phenotypes among Sophophora fruit flies. Our data indicates that the coordinated expression of two melanin synthesis enzymes, Yellow and Tan, recently evolved through novel CRE activities that respond to the spatial patterning inputs of Hox proteins and the sex-specific input of Bric-à-brac transcription factors. Once established, it seems that these newly evolved activities were repeatedly modified by evolutionary changes in the network's trans-regulators to generate large-scale changes in pigment pattern. By elucidating how yellow and tan are connected to the web of abdominal trans-regulators, we discovered that the yellow and tan abdominal CREs are composed of distinct regulatory inputs that exhibit contrasting responses to the same Hox proteins and Hox cofactors. These results provide an example in which CRE origination underlies a recently evolved novel trait, and highlights how coordinated expression patterns can evolve in parallel through the generation of unique regulatory linkages.

No MeSH data available.


Related in: MedlinePlus