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Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera

Liénard, Marjorie LU orcid ; Strandh, Maria LU ; Hedenström, Erik ; Johansson, Tomas LU and Löfstedt, Christer LU (2008) In BMC Evolutionary Biology 8(e270). p.1-15
Abstract
Background: Moths have evolved highly successful mating systems, relying on species-specific mixtures of sex pheromone components for long-distance mate communication. Acyl-CoA desaturases are key enzymes in the biosynthesis of these compounds and to a large extent they account for the great diversity of pheromone structures in Lepidoptera. A novel desaturase gene subfamily that displays Delta 11 catalytic activities has been highlighted to account for most of the unique pheromone signatures of the taxonomically advanced ditrysian species. To assess the mechanisms driving pheromone evolution, information is needed about the signalling machinery of primitive moths. The currant shoot borer, Lampronia capitella, is the sole reported primitive... (More)
Background: Moths have evolved highly successful mating systems, relying on species-specific mixtures of sex pheromone components for long-distance mate communication. Acyl-CoA desaturases are key enzymes in the biosynthesis of these compounds and to a large extent they account for the great diversity of pheromone structures in Lepidoptera. A novel desaturase gene subfamily that displays Delta 11 catalytic activities has been highlighted to account for most of the unique pheromone signatures of the taxonomically advanced ditrysian species. To assess the mechanisms driving pheromone evolution, information is needed about the signalling machinery of primitive moths. The currant shoot borer, Lampronia capitella, is the sole reported primitive non-ditrysian moth known to use unsaturated fatty-acid derivatives as sex-pheromone. By combining biochemical and molecular approaches we elucidated the biosynthesis paths of its main pheromone component, the (Z,Z)-9,11-tetradecadien-1-ol and bring new insights into the time point of the recruitment of the key Delta 11-desaturase gene subfamily in moth pheromone biosynthesis. Results: The reconstructed evolutionary tree of desaturases evidenced two ditrysian-specific lineages (the Delta 11 and Delta 9 (18C>16C)) to have orthologs in the primitive moth L. capitella despite being absent in Diptera and other insect genomes. Four acyl-CoA desaturase cDNAs were isolated from the pheromone gland, three of which are related to Delta 9-desaturases whereas the fourth cDNA clusters with Delta 11-desaturases. We demonstrated that this transcript (Lca-KPVQ) exclusively accounts for both steps of desaturation involved in pheromone biosynthesis. This enzyme possesses a Z11-desaturase activity that allows transforming the palmitate precursor (C16:0) into (Z)-11-hexadecenoic acid and the (Z)-9-tetradecenoic acid into the conjugated intermediate (Z, Z)-9,11-tetradecadienoic acid. Conclusion: The involvement of a single Z11-desaturase in pheromone biosynthesis of a non-ditrysian moth species, supports that the duplication event leading to the origin of the Lepidoptera-specific Delta 11-desaturase gene subfamily took place before radiation of ditrysian moths and their divergence from other heteroneuran lineages. Our findings uncover that this novel class of enzymes affords complex combinations of unique unsaturated fatty acyl-moieties of variable chain-lengths, regio- and stereo-specificities since early in moth history and contributes a notable innovation in the early evolution of moth-pheromones. (Less)
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author
; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
BMC Evolutionary Biology
volume
8
issue
e270
pages
1 - 15
publisher
BioMed Central (BMC)
external identifiers
  • wos:000260951000001
  • scopus:56349161104
  • pmid:18831750
ISSN
1471-2148
DOI
10.1186/1471-2148-8-270
project
The pheromone brewery
language
English
LU publication?
yes
id
88aa40da-e45a-4887-bb61-c65b4ec49736 (old id 1308795)
date added to LUP
2016-04-01 14:35:17
date last changed
2022-04-06 19:23:40
@article{88aa40da-e45a-4887-bb61-c65b4ec49736,
  abstract     = {{Background: Moths have evolved highly successful mating systems, relying on species-specific mixtures of sex pheromone components for long-distance mate communication. Acyl-CoA desaturases are key enzymes in the biosynthesis of these compounds and to a large extent they account for the great diversity of pheromone structures in Lepidoptera. A novel desaturase gene subfamily that displays Delta 11 catalytic activities has been highlighted to account for most of the unique pheromone signatures of the taxonomically advanced ditrysian species. To assess the mechanisms driving pheromone evolution, information is needed about the signalling machinery of primitive moths. The currant shoot borer, Lampronia capitella, is the sole reported primitive non-ditrysian moth known to use unsaturated fatty-acid derivatives as sex-pheromone. By combining biochemical and molecular approaches we elucidated the biosynthesis paths of its main pheromone component, the (Z,Z)-9,11-tetradecadien-1-ol and bring new insights into the time point of the recruitment of the key Delta 11-desaturase gene subfamily in moth pheromone biosynthesis. Results: The reconstructed evolutionary tree of desaturases evidenced two ditrysian-specific lineages (the Delta 11 and Delta 9 (18C>16C)) to have orthologs in the primitive moth L. capitella despite being absent in Diptera and other insect genomes. Four acyl-CoA desaturase cDNAs were isolated from the pheromone gland, three of which are related to Delta 9-desaturases whereas the fourth cDNA clusters with Delta 11-desaturases. We demonstrated that this transcript (Lca-KPVQ) exclusively accounts for both steps of desaturation involved in pheromone biosynthesis. This enzyme possesses a Z11-desaturase activity that allows transforming the palmitate precursor (C16:0) into (Z)-11-hexadecenoic acid and the (Z)-9-tetradecenoic acid into the conjugated intermediate (Z, Z)-9,11-tetradecadienoic acid. Conclusion: The involvement of a single Z11-desaturase in pheromone biosynthesis of a non-ditrysian moth species, supports that the duplication event leading to the origin of the Lepidoptera-specific Delta 11-desaturase gene subfamily took place before radiation of ditrysian moths and their divergence from other heteroneuran lineages. Our findings uncover that this novel class of enzymes affords complex combinations of unique unsaturated fatty acyl-moieties of variable chain-lengths, regio- and stereo-specificities since early in moth history and contributes a notable innovation in the early evolution of moth-pheromones.}},
  author       = {{Liénard, Marjorie and Strandh, Maria and Hedenström, Erik and Johansson, Tomas and Löfstedt, Christer}},
  issn         = {{1471-2148}},
  language     = {{eng}},
  number       = {{e270}},
  pages        = {{1--15}},
  publisher    = {{BioMed Central (BMC)}},
  series       = {{BMC Evolutionary Biology}},
  title        = {{Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera}},
  url          = {{http://dx.doi.org/10.1186/1471-2148-8-270}},
  doi          = {{10.1186/1471-2148-8-270}},
  volume       = {{8}},
  year         = {{2008}},
}