Ipsdienol Dehydrogenase (IDOLDH), a Novel Oxidoreductase Important in the Last Steps of Pheromone Biosynthesis in Ips Spp. (Coleoptera: Scolytinae: Curculionidae)

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Figueroa-Teran, Rubi D.

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2011

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Dissertation

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Bark Beetles , Ipsdienol dehydrogenase , Ips pini , monoterpene dehydrogenase , Pheromone , Short chain dehydrogenase/reductase (SDR)

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Ips spp. beetles biosynthesize ipsdienol and ipsenol in different enantiomeric blends and ratios as pheromones. In order to understand how these beetles evolved the ability to use the same components to synthesize different pheromone blends, the last steps of ipsdienol and ipsenol biosynthesis, which are probably catalyzed by oxidoreductases, must be characterized. Here I report the isolation of ipsdienol dehydrogenase (IDOLDH) from the three bark beetles (Coleoptera): western Ips pini (wIDOLDH), I. confusus (IcIDOLDH) and eastern I. pini (eIpIDOLDH). IDOLDH is the first characterized non-dipteran insect monoterpene short-chain dehydrogenase/reductase (SDR). Quantitative real-time PCR experiments showed that wIDOLDH transcript was induced by feeding in male midguts, the hallmark of pheromone biosynthetic genes. Surprisingly, protein levels were unaffected by feeding, suggesting other factor(s) control pheromone biosynthesis. IDOLDH was present only in male midguts, not in females or other tissues. Functional characterization of wIDOLDH and IcIDOLDH provide the first direct evidence for ipsenol biosynthesis through ketone intermediates and interconversion of (-)-ipsdienol to ipsdienone. WIpIDOLDH oxidized racemic and (-)-ipsdienol to ipsdienone and reduced ipsdienone to (-)-ipsdienol and ipsenone to (-)-ipsenol, but discriminated against (+)- ipsdienol as a substrate. IcIDOLDH similarly oxidized (-)-ipsdienol to ipsdienone, discriminated against (+)-ipsdienol, reduced ipsdienone to ipsdienol (stereochemistry not determined), and used ipsenone as a substrate. Ongoing studies showed eIpIDOLDH had similar activities. Kinetic analysis of IDOLDH oxidation of (-)-ipsdienol with NADP⁺ followed the Michaelis-Menton model, indicating this type of analysis is adequate to characterize IDOLDH catalyzed reactions. The expression profiles and conservation of activities across three species strongly supports that IDOLDH has evolved specifically for pheromone biosynthesis in Ips beetles. The functional data indicates that IDOLDH contributes to, but does not solely control the enantiomeric blend of ipsdienol in Ips spp. Additionally, ipsenone was not a reduction product of ipsdienone, suggesting an ipsenone reductase (IDONER) is required for ipsenone biosynthesis. IDOLDH’s primary structure contains all the critical motifs of an alcohol dehydrogenase in the SDR superfamily. Primary sequence identity of IDOLDH isozymes was not as high as expected for sibling species (82%), however the substrate binding loop was highly identical (99%) and the fact that they retain similar substrate profiles suggest that the differences are not important in determining function. Primary sequence comparisons with the human L-3-hydroxyacyl-CoA dehydrogenase type II/ amyloid-β binding alcohol dehydrogenase (hHADH II/ ABAD) showed a much lower identity (36%) but was still surprisingly high for such diverse organisms with different substrate preferences. Although the overall architecture of these enzymes is similar the substrate binding loop regions are completely different, except for the anchor portions, suggesting that much of the substrate specificity differences are probably found in this region. This work adds to our overall understanding of monoterpene and insect SDRs. The data in this dissertation allow the prediction that Ips beetles probably attain their final pheromone blends by the interplay between pheromone biosynthetic enzymes including IDOLDH, myrcene hydroxylase, (+)-ipsdienol oxidoreductase (unidentified), and ipsdienone reductase (unidentified), whose activities are probably controlled by the redox state of the cell. Additionally, this work provides a solid foundation for future studies on insect SDRs and their involvement in pheromone biosynthesis. Future work to identify, model, and kinetically characterize, other pheromone biosynthetic genes will provide a map for understanding how insects have evolved the ability to tune pheromone blends, and aid in identification of targets for pest management.

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