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A Novel Fatty Acyl Desaturase from the Pheromone Glands of Ctenopseustis Obliquana and C. Herana with Specific Z5-Desaturase Activity on Myristic Acid

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A Novel Fatty Acyl Desaturase from the Pheromone Glands of Ctenopseustis Obliquana and C. Herana with Specific Z5-Desaturase Activity on Myristic Acid J Chem Ecol (2014) 40:63–70 DOI 10.1007/s10886-013-0373-1 A Novel Fatty Acyl Desaturase from the Pheromone Glands of Ctenopseustis obliquana and C. herana with Specific Z5-Desaturase Activity on Myristic Acid Åsa K. Hagström & Jérôme Albre & Leah K. Tooman & Amali H. Thirmawithana & Jacob Corcoran & Christer Löfstedt & Richard D. Newcomb Received: 16 September 2013 /Revised: 15 November 2013 /Accepted: 11 December 2013 /Published online: 11 January 2014 # The Author(s) 2014. This article is published with open access at Springerlink.com Abstract Sexual communication in the Lepidoptera typically Planotortrix, with one differentially regulated to produce the involves a female-produced sex pheromone that attracts males distinct blends used by individual species. However, none of the same species. The most common type of moth sex were able to conduct the Δ5-desaturation observed in pheromone comprises individual or blends of fatty acyl deriv- C. herana, and presumably C. obliquana. We have now iden- atives that are synthesized by a specific enzymatic pathway in tified an additional desaturase gene, desat7, expressed in the the female’s pheromone gland, often including a desaturation pheromone glands of both Ctenopseustis species, which is not step. This reaction is catalyzed by fatty acyl desaturases that closely related to any previously described moth pheromone introduce double bonds at specific locations in the fatty acid desaturase. The encoded enzyme displays Δ5-desaturase ac- precursor backbone. The two tortricid moths, Ctenopseustis tivity on myristic acid when heterologously expressed in obliquana and C. herana (brown-headed leafrollers), which yeast, but is not able to desaturate any other fatty acid (C8– are endemic in New Zealand, both use (Z)-5-tetradecenyl C16). We conclude that desat7 represents a new group of acetate as part of their sex pheromone. In C. herana, (Z)-5- desaturases that has evolved a role in the biosynthesis of sex tetradecenyl acetate is the sole component of the pheromone. pheromones in moths. Labeling experiments have revealed that this compound is produced via an unusual Δ5-desaturation of myristic acid. Keywords Pheromone biosynthesis . Ctenopseustis . Fatty Previously six desaturases were identified from the phero- acyl desaturase . Tortricidae . Tetradecanoic acid mone glands of Ctenopseustis and its sibling genus Electronic supplementary material The online version of this article Introduction (doi:10.1007/s10886-013-0373-1) contains supplementary material, which is available to authorized users. The ability of potential mates to locate one another is essential Å. K. Hagström (*) : C. Löfstedt in sexually-reproducing species. Most Lepidoptera use a so- Pheromone Group, Department of Biology, Lund University, phisticated chemical communication system for localization, Sölvegatan 37, 223 62 Lund, Sweden where female moths emit volatile sex pheromones that attract e-mail: [email protected] conspecific males. Generally moths utilize multi-component J. Albre : L. K. Tooman : A. H. Thirmawithana : J. Corcoran : pheromone blends consisting of fatty acid derivatives, usually R. D. Newcomb alcohols, aldehydes, or acetates (Blomquist et al. 2005; The New Zealand Institute for Plant & Food Research Limited, Tillman et al. 1999), which are synthesized in a specialized Auckland, New Zealand abdominal pheromone gland in female moths. Fatty acids J. Albre : L. K. Tooman : R. D. Newcomb such as stearic and palmitic acid are processed by various The Allan Wilson Centre for Molecular Ecology and Evolution, enzymes, the first of which are generally fatty acyl desaturases University of Auckland, Auckland, New Zealand that introduce one or more double bonds at specific locations in the carbon chain (Blomquist et al. 2005;Jurenka2004). The J. Corcoran : R. D. Newcomb The School of Biological Sciences, University of Auckland, fatty acyl desaturases that are used in pheromone biosynthesis Auckland, New Zealand generally are thought to have evolved from a conserved 64 J Chem Ecol (2014) 40:63–70 metabolic Δ9-desaturase that exists in all eukaryotes (Liu 14:OAc present in the sex pheromone (Albre et al. 2012). The et al. 1999). Moths have an additional Δ9-desaturase that sole pheromone component used by C. herana, Z5-14:OAc is prefers oleic acid over palmitic acid compared to the metabol- synthesized directly from tetradecanoic (myristic) acid by Δ5- ic desaturases, which prefer palmitic over oleic acid (Park desaturation, followed by reduction and acetylation (Foster and et al. 2008; Rodriguez et al. 2004). The largest desaturase Roelofs 1996). A similar pathway presumably is responsible lineage in moths comprises the Δ11-desaturases that contain for the biosynthesis of Z5-14:OAc in C. obliquana, but this has many enzymes involved in pheromone biosynthesis. The not been investigated, and in neither species has the desaturase origin of this lineage, presumably from Δ9-desaturases, pre- gene encoding a Δ5-desaturase been discovered. dates the radiation of the ditrysian moths (Liénard et al. 2008), In this study, we identified and functionally characterized a and its expansion has resulted in the evolution of many new novel desaturase gene (desat7) expressed in the pheromone desaturases, some with altered activities, that are used to glands of female C. obliquana and C. herana. When the produce sex pheromone components in moths (for examples desaturase encoded by this enzyme was heterologously see Ding et al. 2011; Liénard et al. 2010). Chain shortening of expressed in yeast, it was found to display a unique Δ5- fatty acyl moieties before or after desaturation is postulated to desaturase activity on myristic acid to produce Z5-14:Acyl. be catalyzed by one or several β-oxidases. The acids then are reduced to alcohols by fatty acyl reductases (Moto et al. 2004), the alcohols transformed to aldehydes by an alcohol Methods and Materials oxidase (Teal and Tumlinson 1986), and acetates produced by acetyl transferase activity (Jurenka 2004). Insects and Chemicals The superfamily Tortricidae is a group of leafroller moths distributed throughout the world, and includes many species C. obliquana,and C. heranawere obtained from Plant & Food that are pests of various crops. The brown-headed and green- Research (previously HortResearch and before that DSIR) headed leafrollers of the genera endemic in New Zealand, insect rearing facility at the Mt Albert Research Centre, Ctenopseustis and Planotortrix, respectively, contain species Auckland, New Zealand. The history of these strains is re- that are pests of horticultural crops (Wearing et al. 1991). The ported in Newcomb and Gleeson (1998). Insects were reared sex pheromones used by species within these genera have on a 16:8 hr l:D cycle, with larvae reared at 20 °C, and pupae attracted considerable attention due to their use of monounsat- and adults at 18 °C. Larvae were reared individually on a urated acetates with double bonds in the Z configuration at general-purpose diet as described in Albre et al. (2012). positions that are unusual compared with pheromones compo- Tetradecanoic acid (14:COOH) was bought from Larodan nents of other moths, including those within the Tortricidae. Fine Chemicals AB (Limhamn, Sweden) and contained no These components include tetra- and hexadecenyl acetates with detectable amounts of Δ5 unsaturated tetradecenoic acid. desaturation at the 5, 7, 8, 9, and 10 positions (Clearwater et al. Methyl esters of (Z)-5 and (E)-5-tetradecenoate (Z5-14:ME 1991;Fosteretal.1991; Foster and Roelofs 1987; Young et al. and E5-14:ME) were synthesized from their corresponding 1996), whereas the 11 position commonly is utilized in other alcohols (purchased from Pherobank) as described in tortricid moths (Blomquist et al. 2005;Jurenka2004). Lassance et al. (2010). Within Ctenopseustis, C. obliquana uses a binary phero- mone of (Z)-8-tetradecenyl acetate (Z8-14:OAc) and (Z)-5- Identification of desat7, Phylogenetic Analysis, tetradecenyl acetate (Z5-14:OAc) in a 4:1 ratio (Clearwater and Bioinformatics et al. 1991;Youngetal.1985), whereas C. herana uses Z5- 14:OAc as its sole pheromone component (Foster and Roelofs The procedures for the isolation of RNA and DNA are de- 1996). In C. obliquana, Z8-14:OAc is biosynthesized from scribed in Albre et al. (2012). Briefly, pheromone glands of 2– stearic acid (18:Acyl) that is chain shortened to 16:Acyl, 3 day-old virgin females were dissected on ice and stored at followed by Δ10-desaturation to produce the intermediate −80 °C. RNA was extracted using a modified trizol method Z10-16:Acyl moiety, which is further chain shortened to Z8- (Life Technologies, Carlsbad, CA, USA) and used as template 14:Acyl before reduction and final acetylation (Foster and for the construction of RNAseq libraries using Illumina’s Roelofs 1988). To date, six desaturases have been identified standard protocols, and sequenced at Macrogen (Seoul, as expressed within the pheromone gland of Ctenopseustis and South Korea). Resulting sequences were assembled and made Planotortrix species, including two Δ9-, a Δ10-, a Δ6- available as blast sets for further analysis. Blast searches using desaturase, a terminal desaturase, and a desaturase thought to a range of insect desaturase sequences then were performed to be non-functional (Albre et al. 2012; Hao et al. 2002). In identify any further desaturases not previously described in C. herana, desat5, which encodes the Δ10-desaturase, is Albre et al. (2012). Novel desaturases that were identified down-regulated in the pheromone gland, resulting in no Z8- were made full length using RACE, amplified in their entirety J Chem Ecol (2014) 40:63–70 65 from antennal cDNA by PCR and resequenced for 95 °C, 30 sec at 60 °C, and 30 sec at 72 °C. A final dissoci- confirmation. ation curve analysis was added (15 sec at 95 °C, 15 sec at For phylogenetic analyses, a common lepidopteran Δ11- 60 °C, and a gradual heating to 95 °C at 0.01 °C/sec) to desaturase (JX679209) from the turnip moth Agrotis segetum determine the purity of the products.
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