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Sex- and tissue-specific profiles of chemosensory gene expression in a herbivorous gall-inducing fly (Diptera: Cecidomyiidae)

Andersson, Martin N LU ; Videvall, Elin LU ; Walden, Kimberley KO; Harris, Marion O; Robertson, Hugh M and Löfstedt, Christer LU (2014) In BMC Genomics 15. p.1-19
Abstract
Background: The chemical senses of insects mediate behaviors that are closely linked to survival and reproduction.

The order Diptera contains two model organisms, the vinegar fly Drosophila melanogaster and the mosquito

Anopheles gambiae, whose chemosensory genes have been extensively studied. Representing a third dipteran

lineage with an interesting phylogenetic position, and being ecologically distinct by feeding on plants, the Hessian

fly (Mayetiola destructor Say, Diptera: Cecidomyiidae) genome sequence has recently become available. Among

plant-feeding insects, the Hessian fly is unusual in ‘reprogramming’ the plant to create a superior food and in being the

target of plant... (More)
Background: The chemical senses of insects mediate behaviors that are closely linked to survival and reproduction.

The order Diptera contains two model organisms, the vinegar fly Drosophila melanogaster and the mosquito

Anopheles gambiae, whose chemosensory genes have been extensively studied. Representing a third dipteran

lineage with an interesting phylogenetic position, and being ecologically distinct by feeding on plants, the Hessian

fly (Mayetiola destructor Say, Diptera: Cecidomyiidae) genome sequence has recently become available. Among

plant-feeding insects, the Hessian fly is unusual in ‘reprogramming’ the plant to create a superior food and in being the

target of plant resistance genes, a feature shared by plant pathogens. Chemoreception is essential for reproductive

success, including detection of sex pheromone and plant-produced chemicals by males and females, respectively.

Results: We identified genes encoding 122 odorant receptors (OR), 28 gustatory receptors (GR), 39 ionotropic

receptors (IR), 32 odorant binding proteins, and 7 sensory neuron membrane proteins in the Hessian fly genome. We

then mapped Illumina-sequenced transcriptome reads to the genome to explore gene expression in male and female

antennae and terminal abdominal segments. Our results reveal that a large number of chemosensory genes have

up-regulated expression in the antennae, and the expression is in many cases sex-specific. Sex-specific expression is

particularly evident among the Or genes, consistent with the sex-divergent olfactory-mediated behaviors of the adults.

In addition, the large number of Ors in the genome but the reduced set of Grs and divergent Irs suggest that the

short-lived adults rely more on long-range olfaction than on short-range gustation. We also report up-regulated

expression of some genes from all chemosensory gene families in the terminal segments of the abdomen, which

play important roles in reproduction.

Conclusions: We show that a large number of the chemosensory genes in the Hessian fly genome have sex- and

tissue-specific expression profiles. Our findings provide the first insights into the molecular basis of chemoreception in

plant-feeding flies, representing an important advance toward a more complete understanding of olfaction in Diptera

and its links to ecological specialization. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
BMC Genomics
volume
15
pages
19 pages
publisher
BioMed Central
external identifiers
  • wos:000340635100001
  • scopus:84902745683
ISSN
1471-2164
DOI
10.1186/1471-2164-15-501
project
Sex pheromone biosynthesis and odorant receptors in gall midges
language
English
LU publication?
yes
id
51386e20-0de1-4559-8c6c-aad4a71cbe24 (old id 4529823)
date added to LUP
2014-07-01 11:41:27
date last changed
2017-09-24 04:01:14
@article{51386e20-0de1-4559-8c6c-aad4a71cbe24,
  abstract     = {Background: The chemical senses of insects mediate behaviors that are closely linked to survival and reproduction.<br/><br>
The order Diptera contains two model organisms, the vinegar fly Drosophila melanogaster and the mosquito<br/><br>
Anopheles gambiae, whose chemosensory genes have been extensively studied. Representing a third dipteran<br/><br>
lineage with an interesting phylogenetic position, and being ecologically distinct by feeding on plants, the Hessian<br/><br>
fly (Mayetiola destructor Say, Diptera: Cecidomyiidae) genome sequence has recently become available. Among<br/><br>
plant-feeding insects, the Hessian fly is unusual in ‘reprogramming’ the plant to create a superior food and in being the<br/><br>
target of plant resistance genes, a feature shared by plant pathogens. Chemoreception is essential for reproductive<br/><br>
success, including detection of sex pheromone and plant-produced chemicals by males and females, respectively.<br/><br>
Results: We identified genes encoding 122 odorant receptors (OR), 28 gustatory receptors (GR), 39 ionotropic<br/><br>
receptors (IR), 32 odorant binding proteins, and 7 sensory neuron membrane proteins in the Hessian fly genome. We<br/><br>
then mapped Illumina-sequenced transcriptome reads to the genome to explore gene expression in male and female<br/><br>
antennae and terminal abdominal segments. Our results reveal that a large number of chemosensory genes have<br/><br>
up-regulated expression in the antennae, and the expression is in many cases sex-specific. Sex-specific expression is<br/><br>
particularly evident among the Or genes, consistent with the sex-divergent olfactory-mediated behaviors of the adults.<br/><br>
In addition, the large number of Ors in the genome but the reduced set of Grs and divergent Irs suggest that the<br/><br>
short-lived adults rely more on long-range olfaction than on short-range gustation. We also report up-regulated<br/><br>
expression of some genes from all chemosensory gene families in the terminal segments of the abdomen, which<br/><br>
play important roles in reproduction.<br/><br>
Conclusions: We show that a large number of the chemosensory genes in the Hessian fly genome have sex- and<br/><br>
tissue-specific expression profiles. Our findings provide the first insights into the molecular basis of chemoreception in<br/><br>
plant-feeding flies, representing an important advance toward a more complete understanding of olfaction in Diptera<br/><br>
and its links to ecological specialization.},
  articleno    = {501},
  author       = {Andersson, Martin N and Videvall, Elin and Walden, Kimberley KO and Harris, Marion O and Robertson, Hugh M and Löfstedt, Christer},
  issn         = {1471-2164},
  language     = {eng},
  pages        = {1--19},
  publisher    = {BioMed Central},
  series       = {BMC Genomics},
  title        = {Sex- and tissue-specific profiles of chemosensory gene expression in a herbivorous gall-inducing fly (Diptera: Cecidomyiidae)},
  url          = {http://dx.doi.org/10.1186/1471-2164-15-501},
  volume       = {15},
  year         = {2014},
}