Natural Variation of ebony Gene Controlling Thoracic Pigmentation in Drosophila melanogaster

Takahashi, Aya; Takahashi, Kuniaki; Ueda, Ryo; Takano-Shimizu, Toshiyuki

doi:10.1534/genetics.107.075283

Cited by 43 publications

(51 citation statements)

References 28 publications

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“…Studies in Drosophila and Tribolium have shown that ebony plays the central role in suppressing black pigmentation (Figure 1). On loss of function of ebony, a global darkening of body pigmentation was observed in both species (Wittkopp et al 2002b;Takahashi et al 2007;Tomoyasu et al 2009). Based on these observations, we expected ebony RNAi Oncopeltus adults to exhibit black coloration throughout the body.…”

Section: Melanin Patterning In Oncopeltus 405mentioning

confidence: 99%

A Pathway Analysis of Melanin Patterning in a Hemimetabolous Insect

et al. 2016

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Diversity in insect pigmentation, encompassing a wide range of colors and spatial patterns, is among the most noticeable features distinguishing species, individuals, and body regions within individuals. In holometabolous species, a significant portion of such diversity can be attributed to the melanin synthesis genes, but this has not been formally assessed in more basal insect lineages. Here we provide a comprehensive analysis of how a set of melanin genes (ebony, black, aaNAT, yellow, and tan) contributes to the pigmentation pattern in a hemipteran, Oncopeltus fasciatus. For all five genes, RNA interference depletion caused alteration of black patterning in a region-specific fashion. Furthermore, the presence of distinct nonblack regions in forewings and hindwings coincides with the expression of ebony and aaNAT in these appendages. These findings suggest that the region-specific phenotypes arise from regional employment of various combinations of the melanin genes. Based on this insight, we suggest that melanin genes are used in two distinct ways: a "painting" mode, using predominantly melanin-promoting factors in areas that generally lack black coloration, and, alternatively, an "erasing" mode, using mainly melanin-suppressing factors in regions where black is the dominant pigment. Different combinations of these strategies may account for the vast diversity of melanin patterns observed in insects.KEYWORDS Oncopeltus fasciatus; insect pigmentation; melanin patterning; melanin-promoting factors; melanin suppressors P IGMENT patterns are among the most striking and variable features of insect morphology. An extraordinary diversity in coloration distinguishes species, populations within species, individuals within populations, and different body regions (Wittkopp and Beldade 2009). Most insights into the mechanisms underlying such diversity have come from studies on melanization in Drosophila (Wittkopp et al. 2003;Wittkopp and Beldade 2009). Melanization is the pigmentation process wherein precursors (catecholamines) are converted into pigment molecules that are incorporated into the cuticle (Wittkopp and Beldade 2009). These studies have helped to identify a network of melanin genes and their roles in body color patterning (Wright 1987;Wittkopp et al. 2003;Wittkopp and Beldade 2009). The core part of this proposed pathway is shown in Figure 1. The pathway begins with the conversion of tyrosine to dihydroxyphenylalanine (DOPA). DOPA can then be used in two different manners: to produce DOPA melanin (black) or to be converted to dopamine, another precursor of black melanin. In the conversions from DOPA/dopamine to black melanin, the yellow gene is thought to play an essential role in promoting these processes. However, it is still unclear whether yellow plays a role in producing DOPA melanin, dopamine melanin, or both (question marks in Figure 1). Alternatively, production of dopamine melanin can be suppressed by converting dopamine to N-b-alanyldopamine (NBAD) or N-acetyldopamine (NADA). The NBAD bran...

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Section: Melanin Patterning In Oncopeltus 405mentioning

confidence: 99%

A Pathway Analysis of Melanin Patterning in a Hemimetabolous Insect

et al. 2016

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“…Some direct evidences linking this gene to the thoracic or abdominal pigmentation variation in natural populations were put forward by an associated linkage pattern in the 5' upstream region of this gene (Pool and Aquadro, 2007), a genetic mapping result using two wild-derived dark and light strains (Takahashi et al, 2007), and quantitative comparisons of the transcription levels induced by cisregulatory elements from strains with different pigmentation intensities (Rebeiz et al, 2009). The lower expression of this gene in developing epidermis is associated with darker pigmentation, and the higher expression with lighter pigmentation (Takahashi et al, 2007;Rebeiz et al, 2009). This association is reported in populations from Africa (Rebeiz et al, 2009), Australia (Telonis-Scott et al, 2011, and southern Japan (Takahashi and TakanoShimizu, 2011).…”

Section: Pigmentation Variation In D Melanogastermentioning

confidence: 99%

“…Recent studies have shown that the major causal genetic differences underlying naturally occurring pigmentation variation in D. melanogaster lie in the cisregulatory region of ebony (Pool and Aquadro, 2007;Takahashi et al, 2007;Rebeiz et al, 2009;Telonis-Scott et al, 2011;Takahashi and Takano-Shimizu, 2011). This leads us to a question why ebony, among other structural genes in the melanin biosynthesis pathway, has been subjected to frequent changes or possibly the target of natural selection in this species.…”

Section: Perspectivesmentioning

confidence: 99%

Pigmentation and behavior: potential association through pleiotropic genes in Drosophila

Takahashi

2013

Genes Genet. Syst.

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The molecular basis of pigmentation variation within and among Drosophila species is largely attributed to genes in melanin biosynthesis pathway, which involves dopamine metabolism. Most of the genetic changes underlying pigmentation variations reported to date are changes at the expression levels of the structural genes in the pathway. Within D. melanogaster, changes in cis-regulatory regions of a gene, ebony, are responsible for the naturally occurring variation of the body pigmentation intensity. This gene is also known to be expressed in glia, and many visual and behavioral abnormalities of its mutants have been reported. This implies that the gene has pleiotropic functions in the nervous systems. In this review, current knowledge on pigmentation variation and melanin biosynthesis pathway are summarized, with some focus on pleiotropic features of ebony and other genes in the pathway. A potential association between pigmentation and behavior through such pleiotropic genes is discussed in light of cis-regulatory structure and pleiotropic mutations.

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“…Wittkopp, personal communication), by ebony and yellow in D. elegans and D. gunungcola (S. Yeh and J. True, personal communication), and by ebony in some populations of D. melanogaster (Pool and Aquadro 2007;Takahashi et al 2007). Again, none of these loci make a detectable contribution to the difference in pigmentation between D. m. malerkotliana and D. m. pallens.…”

Section: Resultsmentioning

confidence: 99%

Genetic Basis of Sex-Specific Color Pattern Variation in Drosophila malerkotliana

Hamilton

Frank

et al. 2008

Genetics

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Pigmentation is a rapidly evolving trait that can play important roles in mimicry, sexual selection, thermoregulation, and other adaptive processes in many groups of animals. In Drosophila, pigmentation can differ dramatically among closely related taxa, presenting a good opportunity to dissect the genetic changes underlying species divergence. In this report, we investigate the genetic basis of color pattern variation between two allopatric subspecies of Drosophila malerkotliana, a widespread member of the ananassae species subgroup. In D. malerkotliana malerkotliana, the last three abdominal segments are darkly pigmented in males but not in females, while in D. malerkotliana pallens both sexes lack dark pigmentation. Composite interval mapping in F 2 hybrid progeny shows that this difference is largely controlled by three quantitative trait loci (QTL) located on the 2L chromosome arm, which is homologous to the 3R of D. melanogaster (Muller element E). Using highly recombinant introgression strains produced by repeated backcrossing and phenotypic selection, we show that these QTL do not correspond to any of the candidate genes known to be involved in pigment patterning and synthesis in Drosophila. These results, in combination with similar analyses in other Drosophila species, indicate that different genetic and molecular changes are responsible for the evolution of similar phenotypic traits in different lineages. This feature makes Drosophila color patterns a powerful model for investigating how the genetic basis of trait evolution is influenced by the intrinsic organization of regulatory pathways controlling the development of these traits.

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Natural Variation of ebony Gene Controlling Thoracic Pigmentation in Drosophila melanogaster

Cited by 43 publications

References 28 publications

A Pathway Analysis of Melanin Patterning in a Hemimetabolous Insect

A Pathway Analysis of Melanin Patterning in a Hemimetabolous Insect

Pigmentation and behavior: potential association through pleiotropic genes in <i>Drosophila</i>

Genetic Basis of Sex-Specific Color Pattern Variation in Drosophila malerkotliana

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