Combinatorial Activation and Repression by Seven Transcription Factors Specify Drosophila Odorant Receptor Expression

Jafari, Shadi; Alkhori, Liza; Schleiffer, Alexander; Brochtrup, Anna; Hummel, Thomas; Alenius, Mattias

doi:10.1371/journal.pbio.1001280

Cited by 83 publications

(146 citation statements)

References 39 publications

(41 reference statements)

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“…In Drosophila (unlike mammals) the expression of a given OR in a sensory neuron is not directly involved in glomerular targeting (62). Instead, upstream-acting transcription factors involved in neuronal differentiation separately specify both the downstream expression of a particular OR (63) and the axonal guidance of that neuron to its cognate glomerulus in the brain. In O. nubilalis, both strains possess the same cluster of ORs for pheromone detection.…”

Section: Discussionmentioning

confidence: 99%

Genetic mapping of male pheromone response in the European corn borer identifies candidate genes regulating neurogenesis

Koutroumpa

Groot

Dekker

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The sexual pheromone communication system of moths is a model system for studies of the evolution of reproductive isolation. Females emit a blend of volatile components that males detect at a distance. Species differences in female pheromone composition and male response directly reinforce reproductive isolation in nature, because even slight variations in the species-specific pheromone blend are usually rejected by the male. The mechanisms by which a new pheromone signal-response system could evolve are enigmatic, because any deviation from the optimally attractive blend should be selected against. Here we investigate the genetic mechanisms enabling a switch in male response. We used a quantitative trait locus-mapping approach to identify the genetic basis of male response in the two pheromone races of the European corn borer, Ostrinia nubilalis. Male response to a 99:1 vs. a 3:97 ratio of the E and Z isomers of the female pheromone is governed by a single, sex-linked locus. We found that the chromosomal region most tightly linked to this locus contains genes involved in neurogenesis but, in accordance with an earlier study, does not contain the odorant receptors expressed in the male antenna that detect the pheromone. This finding implies that differences in the development of neuronal pathways conveying information from the antenna, not differences in pheromone detection by the odorant receptors, are primarily responsible for the behavioral response differences among the males in this system. Comparison with other moth species reveals a previously unexplored mechanism by which male pheromone response can change in evolution.Ostrinia nubilalis | Z chromosome | pheromone response | sexual communication | QTL analysis

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Section: Discussionmentioning

confidence: 99%

Genetic mapping of male pheromone response in the European corn borer identifies candidate genes regulating neurogenesis

Koutroumpa

Groot

Dekker

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Given that a receptor gene is expressed in only one class of olfactory neurons (;20 cells) out of >100,000 neurons in the organism, it is very unlikely that each of ;50 ORN classes would possess a unique transcription factor code that is not recapitulated elsewhere in the nervous system. A recent study reported that seven transcription factors from different protein families could combinatorially regulate the expression of several olfactory receptors in the adult antenna (Jafari et al 2012). The MMB/dREAM complex appears to function in a different fashion, as it integrates the effect of transcriptional activators, repressors, and chromatin-modifying proteins in a single complex and acts as an adaptable molecular switch for Or expression.…”

Section: One Receptor Per Neuron: Combination Of Chromatin Accessibilmentioning

confidence: 99%

“…Moreover, negative-feedback regulation from the expressed rhodopsin can provide additional exclusion mechanisms to ensure one rhodopsin per photoreceptor ). In the Drosophila olfactory system, receptor gene expression is driven by combinatorial codes of cis-acting sites that recruit transcriptional activators and repressors without negative feedback being involved (Ray et al 2007Tichy et al 2008;Bai et al 2009;Bai and Carlson 2010;Miller and Carlson 2010;Jafari et al 2012). Based on these studies, transcription factors seem likely to act at two levels on olfactory receptor promoters: first to restrict expression in an organ-specific manner, and then within an organ to restrict expression to one class of neuron.…”

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confidence: 99%

Epigenetic regulation of olfactory receptor gene expression by the Myb–MuvB/dREAM complex

et al. 2012

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In both mammals and insects, an olfactory neuron will usually select a single olfactory receptor and repress remaining members of large receptor families. Here we show that a conserved multiprotein complex, Myb-MuvB (MMB)/dREAM, plays an important role in mediating neuron-specific expression of the carbon dioxide (CO 2 ) receptor genes (Gr63a/Gr21a) in Drosophila. Activity of Myb in the complex is required for expression of Gr63a/ Gr21a and acts in opposition to the histone methyltransferase Su(var)3-9. Consistent with this, we observed repressive dimethylated H3K9 modifications at the receptor gene loci, suggesting a mechanism for silencing receptor gene expression. Conversely, other complex members, Mip120 (Myb-interacting protein 120) and E2F2, are required for repression of Gr63a in inappropriate neurons. Misexpression in mutants is accompanied by an increase in the H3K4me3 mark of active chromatin at the receptor gene locus. Nuclei of CO 2 receptor-expressing neurons contain reduced levels of the repressive subunit Mip120 compared with surrounding neurons and increased levels of Myb, suggesting that activity of the complex can be regulated in a cell-specific manner. Our evidence suggests a model in which olfactory receptors are regulated epigenetically and the MMB/dREAM complex plays a critical role in specifying, maintaining, and modulating the receptor-to-neuron map.

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“…The emerging evidence suggests that OR expression is controlled by dedicated combinations of positively and negatively acting TFs (Clyne et al, 1999a;Ray et al, 2007;Ray et al, 2008;Tichy et al, 2008;Bai et al, 2009;Bai and Carlson, 2010;Jafari et al, 2012;Song et al, 2012). A small number of TFs has been identified that is required to specify expression of OR genes, but how the expression or activity of the TFs themselves is regulated resulting in the broad distribution and intermingled pattern of sensillar subtypes is less well understood.…”

Section: Establishing and Maintaining Olfactory Receptor Expression Imentioning

confidence: 99%

“…In contrast to the repression of Rh5 by Rh6 in yR8 PRs, no evidence for one OR repressing an alternative OR gene has been found in Drosophila (Ray et al, 2007) (but see below for mouse). However, as in yR8 PRs, specification mechanisms do play a role in maintenance: at least some of the TFs involved in specification of OR gene expression are also continuously required for their maintenance (Jafari et al, 2012). Recently, evidence was found for epigenetic control of establishment and maintenance of OR expression in post-mitotic ORNs, which sense CO 2 (Sim et al, 2012).…”

Section: Primermentioning

confidence: 99%

Establishing and maintaining gene expression patterns: insights from sensory receptor patterning

2013

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In visual and olfactory sensory systems with high discriminatory power, each sensory neuron typically expresses one, or very few, sensory receptor genes, excluding all others. Recent studies have provided insights into the mechanisms that generate and maintain sensory receptor expression patterns. Here, we review how this is achieved in the fly retina and compare it with the mechanisms controlling sensory receptor expression patterns in the mouse retina and in the mouse and fly olfactory systems.

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Combinatorial Activation and Repression by Seven Transcription Factors Specify Drosophila Odorant Receptor Expression

Abstract: A systematic analysis reveals a regulatory network controlling selective odorant receptor expression and neuronal diversity in Drosophila.

Cited by 83 publications

References 39 publications

Genetic mapping of male pheromone response in the European corn borer identifies candidate genes regulating neurogenesis

Genetic mapping of male pheromone response in the European corn borer identifies candidate genes regulating neurogenesis

Epigenetic regulation of olfactory receptor gene expression by the Myb–MuvB/dREAM complex

Establishing and maintaining gene expression patterns: insights from sensory receptor patterning

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